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The British Journal of Radiology logoLink to The British Journal of Radiology
. 2019 Jun 6;92(1099):20180439. doi: 10.1259/bjr.20180439

Systematic radiological approach to utero-ovarian pathologies

Olivera Nikolic 1,2,1,2,, Marijana Basta Nikolic 1,2,1,2, Aleksandar Spasic 1,2,1,2, Mila Milagros Otero-Garcia 3, Sanja Stojanovic 1,2,1,2
PMCID: PMC6636271  PMID: 31169406

Abstract

Ultrasound is the first-line imaging modality for the evaluation of suspected adnexal masses, endometriosis and uterine tumors, whereas MRI is used as a secondary diagnostic tool to better characterize these lesions. The aim of this review is to summarize the latest advances in the imaging of these utero-ovarian pathologies.

Introduction

Female pelvic imaging is potentially challenging for radiologists due to a broad spectrum of differential diagnoses, including benign and malignant neoplasms and non-neoplastic diseases. The imaging of the small pelvic space with the close proximity of pelvic structures is a demanding task when making the correct diagnosis, especially in terms of identifying the mass origin and substantial overlap of imaging features of numerous pathologic entities. The aim of this review is to provide a systematic radiologic approach to the evaluation of endometriosis, adnexal masses and uterine pathologies, including the latest guidelines, classifications and tips for making the accurate diagnosis. Inflammatory-infectious diseases are omitted, as they are beyond the scope of this article.

adnexal masses

Clinical background

Females with clinically suspected adnexal masses, especially if they are combined with high serum levels of cancer antigen 125 (CA-125), need to undergo imaging studies. CA-125 levels are elevated both in patients with ovarian cancer and benign conditions, such as pelvic inflammatory disease, endometriosis, pregnancy, uterine fibroids and normal menstruation. Due to a substantial overlap of clinical features, this marker alone is not recommended for differentiating between benign and malignant adnexal masse.1 It is of great clinical importance to determine the nature of adnexal mass. The extent of the necessary surgery and who should it be performed by, strongly depend on this finding. Benign adnexal masses may be managed conservatively or resected by a general gynecologist, while malignant ones require radical cytoreductive surgery performed by a surgeon with expertise in gynecologic oncology.2–4

Imaging

Ultrasound is the first-line imaging modality for assessing adnexal lesions; however, approximately 20% of lesions are incompletely characterized after ultrasound evaluation.5 Based on ultrasound examinations, adnexal masses can be divided into three categories: (1) benign, (2) malignant, and (3) indeterminate. Indeterminate adnexal mass is the complex one, that cannot be placed into either category, even after color Doppler assessment, or for which the site of origin cannot be established. For females with indeterminate adnexal mass, MRI is the method of choice. In these females, MRI can reduce the number of unnecessary surgeries of benign lesions and the risk of missing malignant lesions.6 In 2010, the European Society of Urogenital Radiology (ESUR), the female pelvic group published guidelines for sonographically indeterminate adnexal masses, which were updated in 2017.2,4

MR conventional sequences

The MRI of the female pelvis begins with conventional sequences (T 1, T 2 and T 1 with fat saturation). It is very accurate for the identification of endometriotic or fatty masses using T 1 and T 1 with fat saturation sequences. Moreover, conventional MRI distinguishes cystic from solid soft tissue components, as solid soft tissue enhances after a gadolinium (Gd) injection.7 If solid tissue is detected within an adnexal lesion, early publications demonstrated that the T 2T2 signal intensity of the solid tissue is useful to distinguish benign from malignant tumors8 because some benign tumors contain fibrous material in their solid tissue, and thus appear with a low T2 weighted signal. According to the literature, the accuracy of MRI to differentiate benign and malignant masses, using only the conventional sequences, is around 80%.3 Perfusion and diffusion sequences can improve the diagnostic accuracy by 25 and 15%, respectively,9 increasing it up to 94.6%.

Diffusion-weighted imaging (DWI)

DWI is based on the analysis of the movement of water molecules in tissues7 and it represents a powerful tool in the evaluation of adnexal masses. However, even the most powerful tools need something to be compared with.

There are several key points which must be kept in mind for DWI. First of all, water has hypointense signal on DWI sequence with high b-values; furthermore, DWI signal intensity of the mass has to be compared to T 2 and apparent diffusion coefficient (ADC) presentations of the mass, and last but not least, there is a significant overlap between ADC values between benign and malignant lesions which makes quantification not useful for assessing adnexal masses.10

DWI is not a “standalone” technique. It is not applied in mature ovarian teratoma and endometrioma, but it has added value in assessing non-fatty, non-hemorrhagic, entirely solid and complex masses. Low T 2 signal combined with low DWI signal and high b-value (800–1200 s/mm2) shows a very high likelihood of benignity.4 (Figure 1).

Figure 1.

Figure 1.

Ovarian fibroma on the right side, typical MRI features—low T 2 and low DWI signal with high b value of 1200. DWI, diffusion-weightedimaging.

The majority of fibromas show low DWI signal, but there are always exceptions to the rule. Presence of abundant collagen-producing fibroblastic cells and a dense network of collagen fibers within the extracellular matrix can restrict the Brownian motion of water molecules.11 (Supplementary Figure 1)

As DWI is only an indicator of cellularity, it is not always helpful in differentiating indeterminate solid adnexal masses or those with a solid component with high signal on the high b-value DWI. These masses can be benign or malignant and contrast enhanced T 1 is required.4

Dynamic contrast enhancement (DCE)

Indeterminate adnexal masses with a solid component should undergo DCE imaging. According to the definitions proposed by Timmerman et al12 based on the International Ovarian Tumor Analysis (ι) the term “solid tissue” includes solid portions, papillary projections and thickened irregular septa. In the study of Thomassin-Naggara et al.13 DCE MRI sequence was acquired and regions of interest (ROIs) were drawn within the solid portion of the ovarian tumor and adjacent external myometrium followed by comparison of T 1CE curve of the solid component of the mass with that of the external myometrium (Supplementary Figure 2). Plane selection is determined by a radiologist or three-dimensionalT 1 image is used. Three types of enhancement patterns were defined, “curve Type 1” - benign, “curve Type 2” - indeterminate and “curve Type 3” - malignant (Supplementary Figure 3). The lesions which show slow rate and low level of enhancement are likely to be benign, while malignant lesions usually show rapid rate and high level of enhancement.4

In 2013, Thomassin-Naggara et al created the ADNEx MR scoring system14 for characterization of adnexal masses that were indeterminate at ultrasound. This system involved previously mentioned curves as well (Supplementary Figure 4). The ADNEx MR scoring system of adnexal masses accurately relays the radiologist’s suspicion of malignancy to the clinician and helps to standardize the reporting of MRI findings, thus improving the patient care. To our knowledge, a multicenter study which involved ADNEx MR scoring system has been finished, but the results have not been published yet.

Indications for MRI of adnexal masses

  • A complex adnexal mass with equivocal malignant features.

  • A pelvic mass of indeterminate origin

  • A mass adjacent to the uterus with equivocal origin

  • A solid adnexal mass.4

Patient preparation

The preparation is quite simple:

  • Fastening 4 h before the examination

  • Urinary bladder half-full

  • Smooth muscle relaxant is given intravenously or intramuscularly.

Diagnostic algorithm

The basic protocol for MRI of adnexal masses includes:

  • T 2 sagittal pelvis

  • T 2, T 1 covering the mass in the same orthogonal plane (axial, coronal or oblique) with identical slice thickness.

Depending on the MRI mass morphology, different problem solving sequences can be included2,4,15

  • T 1 “bright mass” – FST 1 (to confirm/exclude the presence of fat)

  • T 2 “dark” solid mass - oblique T 2 through the maximum point of contact between the mass and the uterus (to determine the anatomic site of origin, ovarian or uterine, and differentiate uterine myoma vs adnexal mass)

  • T 2 “dark” solid mass - DWI is helpful in explaining the nature of the lesion (benign vs malignant)

  • T 2 solid mass (the one that is not dark on T 2) - combination of DWI and CET 1 can help in characterization of the lesion

  • Cystic-solid mass - DWI and CET 1 together may help in characterization of the lesion.

Mri categories

According to MRI morphological features, adnexal masses can be divided into three categories5:

  1. T 1 bright

  2. T 2 solid

  3. Complex cystic masses (Supplementary Figure 5) (Table 1).

Table 1.

MRI categories of adnexal masses

T1 bright T2 solid Cystic-solid
Mature teratoma Leiomyoma Cystadenoma
Hemorrhagic cyst Fibroma/Thecoma Cystadenofibroma
Endometrioma Struma ovarii Borderline tumour
Mucinous cystadenoma Primary cancer Primary cancer
Melanoma metastasis Metastasis Metastasis
Hydrosalpinx
Abscess

T 1 bright masses

Considering T 1 bright masses, there are no new data in the updated ESUR guidelines. To distinguish fat from blood T 1, T 2 and FST 1 sequences are used and if there are some solid components, gadolinium injection is required (Figure 2). MR features that allow the diagnosis of fat are high signal intensity on T 1 and low signal intensity on FST 1 sequence.

Figure 2. .

Figure 2. 

Mature ovarian teratomas - T 1 axial images-bilateral high signal intensity masses (red arrows) with fat suppression on T 1FS (blue arrows), and torsion on the left side - T 1 sagittal image - “whirlpoool sign” (green arrow). Yellow arrow indicates Rokitansky nodule.

T 2 solid masses

Ovarian masses which show low signal intensity on T 2 images require a check-up using DWI. Entirely low signal intensity on DWI images with high b-values shows that the mass is probably benign and contrast enhanced T 1 imaging is unnecessary (Supplementary Figure 6). T 2 solid masses with diffusion restriction and confirmation on ADC map must be evaluated with contrast enhanced sequence after gadolinium injection; if they show contrast enhancement they are probably malignant (Supplementary Figure 7).

Complex cystic or cystic-solid masses

A mixed cystic and solid appearance of an ovarian mass should raise a suspicion of malignancy, like surface epithelial tumors and metastatic lesions. However, benign lesions, like mature cystic teratomas or ovarian dermoid cysts, also appear as a complex mass,16 but they can be diagnosed if the presence of fat is confirmed.

The benchmark MRI technique for malignant features is CET 1, whereas DWI plus DCE MRI are additional diagnostic tools. If the mass shows low DWI signal with high b-values it is probably benign, and it usually has Type 1 curve at DCE MRI. Malignant lesions show Type 3 curve at DCE MRI. Borderline tumors can show indeterminate Type 2 curves at DCE MRI (Figures 3–5) (Supplementary Figure 8).

Figure 3. .

Figure 3. 

Ovarian cystadenocarcinoma - axial T 1 left-sided solid ovarian mass (a), with a cystic component, hyperintense on DWI with high b-value of 1200 (b), strong post-contrast enhancement (c), perfusion curve Type 3 - malignant (d). DWI, diffusion-weighted imaging.

Figure 4.

Figure 4.

Krukenberg tumors - complex solid cystic bilateral ovarian masses, hyperintense on DWI with high b -value of 1200 (a), post-contrast enhancement of solid components (b), Type 3 malignant perfusion curves (c, d). DWI, diffusion-weighted imaging.

Figure 5.

Figure 5.

Mucinous cystadenoma borderline-right-sided heterogenous cystic ovarian mass with solid component T 1FS + C enhancement of solid portion (a), hyperintense solid portion on DWI with high b -value of 1200 (b), Type 2 perfusion curve (c). DWI, diffusion-weighted imaging.

Tips and tricks

  • Ultrasound demonstration of a solid component within a cystic mass is the most important predictor of malignancy.17

  • MRI allows identification of blood products within hemorrhagic masses that may mimic solid tumors at ultrasound.

  • Fat-suppressed T 1 MRI may reveal small amounts of fat, which allows diagnosis of a mature teratoma

  • Contrast-enhanced T 1 MRI depicts features of malignancy such as enhancing mural nodules and/or solid areas with or without necrosis.3

endometriosis

Clinical background

Endometriosis is defined as presence of ectopic functional endometrial glands and stroma outside the uterine cavity, which in most cases causes chronic inflammatory conditions.18 Females affected by endometriosis typically have a spectrum of pelvic and abdominal pain symptoms, ranging from mild to severe dysmenorrhea, dyspareunia, heavy menstrual bleeding, non-menstrual pelvic pain, pain at ovulation, dyschezia and dysuria, as well as chronic fatigue.19 Depending on the location of endometriosis, symptoms may also include rectal bleeding and constipation, or pleural chest pain, pneumothorax, pleural effusions or cyclic hemoptysis in thoracic involvement.20 Endometriosis is an underlying cause in about 1/3 of the patients suffering from chronic pelvic pain,21 and about 25% of female infertility.22

Several pathogenic theories have been proposed including metastatic, metaplastic and induction theory, with metastatic or retrograde menstruation hypothesis being the most convincing model.23

The estimated average prevalence of endometriosis is about 10 per 1000 females, affecting patients during the prime years of their life, with peak incidence at the age of 40.24,25

Classification

Classification of endometriosis has remained controversial and challenging, due to many manifestations of the disease. Usually it involves location, extent and depth of the endometrial implants, presence and severity of adhesions and presence and size of ovarian endometriomas.26 However, in radiological clinical practice, there are three subtypes of endometriosis: ovarian, superficial and deep pelvic endometriosis.27

Endometrioma is a localized form of endometriosis, usually localized on the ovaries. Superficial endometriosis comprises superficial plaques scattered across the peritoneum, ovaries and uterine ligaments, while deep pelvic endometriosis is defined as subperitoneal invasion by endometriotic lesions that exceeds 5 mm in depth.28

Most common sites of endometriosis are the ovaries, pelvis and peritoneum, and the most common sites of pelvic involvement are the pouch of Douglas, uterosacral ligaments and torus uterinus.29 Less common sites of involvement include the cesarean section scar, deep subperitoneal tissue, gastrointestinal (GI) tract, bladder, chest and subcutaneous tissue.

Imaging

Transvaginal ultrasonography (TVUS) is a first-line imaging method, excellent for visualization of ovarian and urinary bladder involvement,30 while transrectal ultrasonography (TRUS) is a useful tool for evaluation of rectovaginal, uterosacral or rectosygmoid involvement.31 Transvaginal ultrasonography displays endometriomas as homogenous, typically unilocular hypoechoic lesions, with no Doppler signal, containing thin or thick septations.32

MRI is considered as a method of choice for evaluation of endometriosis.33 According to ESUR, basic MR protocol for imaging of endometriosis should include at least two orthogonal T 2 planes (axial and most commonly sagittal), T 1 sequence with and without fat suppression, and optional addition of DWI, contrast-enhanced sequence after Gd injection, susceptibility weighted imaging (SWI) and HASTE sequences.34

Endometriomas typically show high signal intensity on T 1 images and a “shading” sign on T 2 images, caused by old blood products, which contain extremely high iron and protein concentrations, accompanied by variable restriction of diffusion35 (Figure 6). Differential diagnosis of endometriomas includes hemorrhagic cysts, which usually have lower signal intensity on T 1 images and absence of a “shading” sign, and cystic teratoma, for which fat suppression is a problem-solving sequence.35 (Figure 7)

Figure 6.

Figure 6.

Endometrioma of the right ovary. Hyperintense lesion on T 1 (a), with typical shading sign on T2 image (b).

Figure 7.

Figure 7.

Kissing ovaries - patognomonic sign of deep pelvic endometriosis.

The presence of an enhancing mural nodule, solid components or thick septations may indicate a malignant transformation of endometriosis.36

Ectopic endometrial foci present with cyclic bleeding, which leads to inflammatory response, fibrous reaction and adhesions.37 These foci or hemorrhagic “powder burn” lesions appear bright on T 1FS sequences, whereas solid deep lesions predominantly present as hypointense nodules on T 2 images, with intermediate to hyperintense signal on T 1 images, depending on the extent of red cell extravasation outside the glandular ducts into the surrounding stroma.38 Due to the smooth muscle proliferation and fibrous tissue, nodules and masses can have irregular or indistinct margins.8 Adhesions and inflammatory reactions commonly lead to occurrence of “kissing ovaries,” hydrosalpinx and hematosalpinx.39 (Figure 8 and Supplementary Figure 9).

Figure 8.

Figure 8.

Patient with history of infertility, administered at ER for ileus. CT showed infiltrative lesion of caecum and terminal ileum (yellow arrow) and right adnexal cystic lesion (red arrow). Operatively confirmed infiltrative ileocecal endometriosis and right ovarian endometrioma.

Uterine ligament involvement shows irregular margins, asymmetry, nodularity and thickening of ligaments, whereas uterosacral ligaments are the most commonly affected. Vaginal endometriosis is a rare condition characterized by a lesion usually located in the posterior fornix or in the upper part of posterior vagina, presenting with hypointense posterior thickening on T 2 images, or as a mural nodule with variable intensity on T 1 images.40 Lesions located at pouch of Douglas are usually ill-defined, hypointense on T 2 images, often leading to partial or complete obliteration of the pouch of Douglas, with presence or absence of suspended or lateralized fluid collection.34,41 (Supplementary Figure 10).

Rectovaginal endometriosis is one of the most severe forms of endometriosis, characterized by nodules or masses that pass through the lower border of the posterior lip of the cervix pulling the vaginal fornix.42,43

The bowel is the most common site of extragenital endometriosis,27 with rectum and rectosigmoid junction being the most frequent bowel locations. MRI can depict bowel wall T 1 hyperintense foci due to hemorrhage, T 2 hyperintense foci due to dilated endometrial glands, rectal wall thickening, the “mushroom sign” (low-signal-intensity of fibrotic endometriosis and hypertrophic muscularis propria surrounded by high-signal-intensity mucosa and submucosa giving a characteristic appearance of mushroom cap), depth of bowel wall infiltration, the length of the affected area and the distance of the lesion from the anus.44 Inflammatory response due to repeated hemorrhage can lead to adhesions, strictures and bowel obstruction. Adhesions are sometimes observed indirectly, as anterior displacement of the rectum, abnormal bowel angulations or loss of fat plane between uterus and bowel.45 (Figure 9)

Figure 9.

Figure 9.

Endometriosis of anterior abdominal wall (yellow arrow) and right ovary (red arrow) - CT (a, b) , MRT 2 (c) and T 1FS (d).

Involvement of the urinary bladder presents as localized or diffuse bladder wall thickening and signal intensity abnormality, nodules or masses usually located at the level of the vesicouterine pouch, while involvement of bladder mucosa is rare.46

Endometriosis of the abdominal wall is the most frequent extrapelvic endometriosis localization, usually occurring at the level of surgical scar following hysterectomy or cesarean section.47 It presents with T 1/T 2 iso- or hyperintense nodular subcutaneous lesion, which may show restricted diffusion (Figure 10).

Figure 10.

Figure 10.

Sagittal T 2 images of submucous (a) and subserous (b) myoma. Axial post contrast CT of degenerated and calcified subserous myomas (c).

Other rare extraperitoneal localizations include pelvic nerve implants, diaphragmatic, pleural and chest involvement.48

Tips and tricks

  • MRI has proven to be a very reliable imaging method in the diagnosis of endometriosis.40,49

  • Visualization of small peritoneal implants or adhesions may be challenging.

  • Direct visualization is facilitated in the presence of fluid, while indirect signs of adhesions are angulated bowel loops, elevated posterior vaginal fornix, changed position of the uterus and ovaries, or triangular pulling of anterior rectal wall.50

  • Diagnostic value of MRI can be further enhanced by incorporating additional sequences such as gradient echo or susceptibility weighted into routine protocol, with application of intravaginal and intrarectal ultrasonic gel contrast or water.

uterine tumors

Leiomyoma

Clinical background

Leiomyomas or fibroids are the most common benign neoplasms of the uterus, arising from the smooth muscle layer and its accompanying connective tissue. It is estimated that about 20–40% of females are diagnosed with leiomyomas, but only a fraction are symptomatic and/or require surgery.51

Imaging

ESUR recommended a protocol52 for MRI using sagittal/oblique T 2 and axial T 1 sequences with additional fast T 2 of upper abdomen for evaluation of large tumors, renal obstruction and metastases. A number of optional sequences are also recommended such as:

  • T 1FS for differential diagnosis of hemorrhagic lesions of the uterus and ovaries;

  • Oblique coronal T 2 for relationship with uterine cavity and evaluation of ovarian or uterine origin;

  • Contrast-enhanced sequence after Gd injection for characterization of leiomyomas and differentiation of leiomyosarcomas (LMS) and adnexal masses;

  • DWI for characterization of atypical leiomyomas.

Leiomyomas usually appear as spherical, well circumscribed, extensive lesions of the uterus. If located peripherally they can bulge the uterine contour. Calcifications are clearly depicted on CT, with mostly peripheral distribution. Appearance of fibroids on MRI is relatively heterogeneous showing T 1 and T 2 hypointense well-circumscribed lesions. T 1 hyperintensity suggests degeneration caused by venous thrombosis. Flow voids are visible on the periphery, and contrast enhancement is variable, usually not intense (Figure 11).

Figure 11.

Figure 11.

Cervical cancer FIGO 2B (a) T 2 axial - solid endocervical mass with stromal ring disruption on the left side-and parametrial invasion. (b) T 1FS + C axial - prominent enhancement of the cervical mass, (c) DWI - hyperintense cervical mass on DWI with high b-value of 1200, (d) DWI – bilateral hyperintense opturatory lymphnodes on DWI with high b-value of 1200, suspected lymphadenopathy. DWI, diffusion-weighted imaging.

In ubiquitous cases, it is not possible to determine the origin of pelvic extensive lesions by ultrasound. MRI showing a claw sign and a bridging vessel sign point to uterine lesion, thus excluding ovarian origin.

Differential diagnosis

The distinction between leiomyomas and adenomyosis is important because of completely different therapeutic approaches. Fibroids tend to be better circumscribed, have pseudocapsules and are usually T 2 hypointense, compared to lack of pseudocapsule in adenomyosis and T 2 isointensity to surrounding myometrium. The use of DWI imaging is reported to have a major role in their differentiation with significant difference in ADC values of these entities with less ADC values in fibroids compared to adenomyosis.51

Cervical cancer

Clinical background

Cervical cancer is a largely preventable disease, but it is one of the leading causes of cancer death in females worldwide. Most deaths occur in low- to middle-income countries. Human papillomavirus (HPV) is the most common infection acquired during sexual relations, usually in early sex life. In most HPV infected females and males, these infections resolve spontaneously. A minority of HPV infections persist. In females, HPV infection may lead to cervical precancerous conditions and if not treated, it may progress to cancer 10 to –20 years later.

Imaging

MRI is the preferred imaging modality which delineates the tumor from the surrounding healthy uterine and cervical tissue, evaluates parametrial invasion and invasion of the surrounding structures, such as bladder and rectum. The utility of the multiparametric approach is limited in patients with cervical cancer, and multiplanar T 2 weighted imaging remains the mainstay of cancer staging. The reported accuracy of T 2 imaging is 83–93% for the diameter of cervical tumors, and 80–87% for assessing parametrial extension.53 On T 2, they appear as relatively hyperintense to the surrounding cervical stroma. T 2 sequences in two planes should be obtained, sagittal and oblique. Oblique images must be acquired perpendicularly to the long axis of the cervical canal.54

Contrast enhanced examination delineates the tumor as a hyperintense lesion and it may be useful in small cervical cancers in fertility sparing surgery (Supplementary Figure 11) (Figure 12). DWI ADC histogram analysis can differentiate Stage 1b cervical cancer from a normal cervix or a cervical benign lesion with high accuracy and it may be helpful in noninvasive distinguishing histologic types and grades of cervical cancer.55

Figure 12.

Figure 12.

Endometrial cancer FIGO IB Grade 2. Hypointense lesion on T 2 and post-contrast images (a, b), infiltrating more than 50% of myometrium depth, with restricted diffusion (c, d).

Nodal involvement does not affect the FIGO staging, but it remains a challenge, especially as it is considered to be a major predictor of survival. The usual imaging parameters, such as the nodular size over 1 cm and presence of necrosis, are evaluated but do not contribute to definitive FIGO stage of the disease.

MRI evaluation is based on FIGO classification, and focuses on tumor size, parametrial invasion, internal os invasion, vaginal invasion, pelvic wall or adjacent organ involvement, as well as lymph node involvement and distant metastases (Supplementary Figure 12), (Figure 13, and Supplementary Figure 13).

Figure 13.

Figure 13.

Carcinosarcoma - T 2 sagittal/coronal/T 2 + DWI/coronal T 1FS + C large heterogeneous mass with endometrial location with intratumoral areas of necrosis, early and persistent post-contrast enhancement (differential diagnosis adenocarcinoma - hypovascular). DWI, diffusion-weighted imaging.

On follow-up, MRI features of good response to treatment include significant decrease in tumor size 2 months after initiation of the therapy (Supplementary Figure 14), increased tumor ADC values on DWI 2 weeks after initiation of radiotherapy, and changes in quantitative pharmacokinetic parameters on DCE-MRI during the course of early (after 20–25 Gy) and mid-term (after 45–50 Gy) radiotherapy treatment.56

Endometrial cancer

Clinical background

Endometrial carcinoma (EC) is the most common genital malignancy in developed countries and the most common malignancy of the female reproductive tract.57 In three out four patients, it affects post-menopausal females. The leading symptom is vaginal bleeding and it is irrelevant whether the bleeding is of minor or major intensity; gynecological examination is mandatory.

Imaging

FIGO suggests that the staging can be done by MRI if available, as the new guidelines recognized MRI as the imaging modality of choice for evaluating disease extent in patients with newly diagnosed endometrial cancer.58 Indications for MRI with proven or suspected endometrial cancer include: high grade, serous or clear cell adenocarcinomas; suspicion of advanced disease, including cervical stroma extension and confirmation of Stage III and IV disease; screening for lymph node enlargement as a roadmap for lymph node sampling; medical contraindication for surgical staging; suspected endometrial cancer with inability of curettage (e.g. cervical stenosis).59

EC is usually hypointense on T 2 imaging compared to the endometrium, and hyperintense in comparison to the adjacent myometrium. In even greater percentage of cases, it can be demarcated on contrast-enhanced imaging as an area of hypointensity, and on DWI as a region of restricted diffusion (Figure 13). Classical criteria for evaluation of nodal metastases among the less specific are the size over 1 cm in the short axis diameter, irregular nodal contour, central area of necrosis and formation of a nodal group.

From an imaging perspective, poor prognostic factors include invasion of the myometrium and cervical stroma, extrauterine spread and lymph node involvement.

Contrast enhanced evaluation has been reported to be useful in the evaluation of myometrial infiltration. Comparing the radiologic and pathologic findings, focal peritumoral enhancement reflects the increased vascularity at the attachment site of the endometrial cancer. Irregular thin-layered peritumoral enhancement reflects the increased vascularity due to stromal reaction at the tumor front of the myometrial invasion. This enhancement is an indication of myometrial invasion and it should not be misinterpreted as subendometrial enhancement.60

However, in the detection of deep myometrial infiltration by EC, MRI examination sequences T 2 and DWI showed better results than contrast enhanced (accuracy 85.7% for T 2 and for DWI vs 82.1% for contrast-enhanced). In particular, DWI showed the highest sensitivity (0.86) in detection of deep myometrial infiltration, whereas T 2 warranted the highest specificity (0.89).61 DWI is not inferior to CET 1 in local staging of EC and offers the main advantage of avoiding endovenous contrast media administration, reducing the costs and increasing patients’ safety.61 In addition to evaluation of a primary tumor, DWI is useful in evaluation of nodal involvement. The combination of nodal relative ADC with the nodal size criterion has increased sensitivity from 25 to 83% in the detection of lymphonodal metastases.62

Multiple studies have shown that combination of imaging sequences, DWI and T 2 or fused image is effective in assessing deep myometrial invasion,63 thus giving rise to the question of contrast media administration necessity during evaluation of EC.

In the end, it is suggested that the sensitivity of MRI in detection of high-risk tumor features is not high enough to allow omission of lymphadenectomy in patients with negative findings. The MRI has a high specificity and favors surgical staging in patients with positive findings. Compared with contrast-enhanced imaging, analysis of curves of enhancement and DWI may be more reliable in the radiological staging of EC.64

Sarcoma

Clinical background

Uterine sarcomas are rare and aggressive mesenchymal tumors accounting for less than 3% of uterine corpus tumors. LMS is the most common histologic subtype, followed by endometrial stromal sarcoma (ESS) and undifferentiated uterine sarcoma. Carcinosarcoma was previously categorized as uterine sarcoma, but now it is classified as high-grade EC.65

The great majority of LMSs arise de novo, but they rarely (in 0.2% of cases) result from a sarcomatous transformation in a benign leiomyoma. It has a 5-year survival rate ranging from 18.8 to 68%, which varies widely according to different stages. The reported risk of recurrence varies from 45 to 73%.65,66

Growth of uterine mass after menopause and elevated lactate dehydrogenaseLDH should be viewed as suspicious for LMS.

Imaging

MRI is the imaging method of choice for uterine sarcomas. No single MR feature can distinguish uterine sarcoma from atypical leiomyoma. Combined MR features may suggest correct diagnosis including large uterine mass with hemorrhage (high signal on T 1 image), heterogeneous high signal on T 2 imaging with central necrosis and infiltrative borders. Rapid early enhancement of solid components and diffusion restriction are noticeable on DCE and DWI sequences. Diffusion restriction can be seen with hypercellular LM and that is why it is not reliable as a standalone technique for making the diagnosis of LMS.67 (Supplementary Figure 15 and Figure 14).

Figure 14.

Figure 14.

Endometrial stromal sarcoma - axial/sagittal and coronal T 2 images show large well delineated endometrial-based tumor with T 2 low intensity bands

Endometrial stromal sarcoma presents as a large endometrial-based tumor (Figure 15). It is well-delineated or with infiltrative borders (T 2 low signal bands and wormlike tumor extension along the vessels or pelvic ligaments) (Supplementary Figure 16).

Figure 15.

Figure 15.

Endometrial stromal sarcoma - DWI “worm-like“ tumor extension along the vessels or ligaments. DWI, diffusion-weighted imaging.

Tips and tricks

  • The presence of claw sign and bridging vessel sign is a key to determine the uterine origin of a mass.

  • High-resolution T 2 images are the mainstay in pelvis MRI. Axial oblique T 2 images must be angled perpendicularly to the endometrium and cervix in endometrial and cervical cancer, respectively.

  • In cervical cancer, MRI can accurately assess the tumor size, parametrial invasion, pelvic sidewall invasion, and lymph node metastasis.

  • In endometrial cancer, MRI is the best tool to assess preoperatively the depth of myometrial invasion and cervical involvement, which correlate with tumor grade, and the presence of lymph node metastases.

  • The clinical features of benign leiomyomas and uterine sarcomas are often indistinguishable. MR features most strongly associated with uterine sarcomas are diffusion restriction, nodular borders, hemorrhage, “T 2 dark” area(s), and central unenhanced areas.

Conclusion

A good clinical background and the use of MRI, as well as other MR techniques, DWI and perfusion or DCE, provide radiologists with the tools necessary to make accurate diagnosis of the numerous female pelvic lesions.

Contributor Information

Olivera Nikolic, Email: olivera.nikolic@mf.uns.ac.rs.

Marijana Basta Nikolic, Email: marijana.bastanikolic@mf.uns.ac.rs.

Aleksandar Spasic, Email: aleksandar.spasic@mf.uns.ac.rs.

Mila Milagros Otero-Garcia, Email: Maria.Milagros.Otero.Garcia@sergas.es.

Sanja Stojanovic, Email: sanja.stojanovic@mf.uns.ac.rs.

REFERENCES

  • 1. Biggs WS , Marks ST . Diagnosis and management of adnexal masses . Am Fam Physician 2016. ; 93 : 676 – 81 . [PubMed] [Google Scholar]
  • 2. Spencer JA , Forstner R , Cunha TM , Kinkel K . ESUR guidelines for MR imaging of the sonographically indeterminate adnexal mass: an algorithmic approach . Eur Radiol 2010. ; 20 : 25 – 35 . doi: 10.1007/s00330-009-1584-2 [DOI] [PubMed] [Google Scholar]
  • 3. Spencer JA , Ghattamaneni S . MR imaging of the sonographically indeterminate adnexal mass . Radiology 2010. ; 256 : 677 – 94 . doi: 10.1148/radiol.10090397 [DOI] [PubMed] [Google Scholar]
  • 4. Forstner R , Thomassin-Naggara I , Cunha TM , Kinkel K , Masselli G , Kubik-Huch R , et al. . ESUR recommendations for MR imaging of the sonographically indeterminate adnexal mass: an update . Eur Radiol 2017. ; 27 : 2248 – 57 . doi: 10.1007/s00330-016-4600-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Sadowski EA , Robbins JB , Rockall AG , Thomassin-Naggara I . A systematic approach to adnexal masses discovered on ultrasound: the ADNEX Mr scoring system . Abdom Radiol 2018. ; 43 : 679 – 95 . doi: 10.1007/s00261-017-1272-7 [DOI] [PubMed] [Google Scholar]
  • 6. Nikolic O , Ostojic J , Basta Nikolic M , Spasic A , Donat D , Stojanovic S . Mr diagnostics of adnexal masses . ECR 2017. ;. [Google Scholar]
  • 7. Thomassin-Naggara I , Balvay D , Rockall A , Carette MF , Ballester M , Darai E , et al. . Added value of assessing adnexal masses with advanced MRI techniques . BioMed Research International 2015. ; 2015 : 1 – 10 . doi: 10.1155/2015/785206 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8. Siegelman ES , Outwater EK . Tissue characterization in the female pelvis by means of MR imaging . Radiology 1999. ; 212 : 5 – 18 . doi: 10.1148/radiology.212.1.r99jl455 [DOI] [PubMed] [Google Scholar]
  • 9. Thomassin-Naggara I , Toussaint I , Perrot N , Rouzier R , Cuenod CA , Bazot M , et al. . Characterization of complex adnexal masses: value of adding perfusion- and diffusion-weighted MR imaging to conventional MR imaging . Radiology 2011. ; 258 : 793 – 803 . doi: 10.1148/radiol.10100751 [DOI] [PubMed] [Google Scholar]
  • 10. Kierans AS , Bennett GL , Mussi TC , Babb JS , Rusinek H , Melamed J , et al. . Characterization of malignancy of adnexal lesions using ADC entropy: comparison with mean ADC and qualitative DWI assessment . J. Magn. Reson. Imaging 2013. ; 37 : 164 – 71 . doi: 10.1002/jmri.23794 [DOI] [PubMed] [Google Scholar]
  • 11. Zhang P , Cui Y , Li W , Ren G , Chu C , Wu X . Diagnostic accuracy of diffusion-weighted imaging with conventional MR imaging for differentiating complex solid and cystic ovarian tumors at 1.5T . World Journal of Surgical Oncology 2012. ; 10 : 237 . doi: 10.1186/1477-7819-10-237 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12. Timmerman D , Valentin L , Bourne TH , Collins WP , Verrelst H , Vergote I , Terms VI . Terms, definitions and measurements to describe the sonographic features of adnexal tumors: a consensus opinion from the international ovarian tumor analysis (iota) group . Ultrasound Obstet Gynecol 2000. ; 16 : 500 – 5 . doi: 10.1046/j.1469-0705.2000.00287.x [DOI] [PubMed] [Google Scholar]
  • 13. Thomassin-Naggara I , Daraï E , Cuenod CA , Rouzier R , Callard P , Bazot M . Dynamic contrast-enhanced magnetic resonance imaging: a useful tool for characterizing ovarian epithelial tumors . J. Magn. Reson. Imaging 2008. ; 28 : 111 – 20 . doi: 10.1002/jmri.21377 [DOI] [PubMed] [Google Scholar]
  • 14. Thomassin-Naggara I , Aubert E , Rockall A , Jalaguier-Coudray A , Rouzier R , Daraï E , et al. . Adnexal masses: development and preliminary validation of an Mr imaging scoring system . Radiology 2013. ; 267 : 432 – 43 . doi: 10.1148/radiol.13121161 [DOI] [PubMed] [Google Scholar]
  • 15. Allen BC , Hosseinzadeh K , Qasem SA , Varner A , Leyendecker JR . Practical approach to MRI of female pelvic masses . American Journal of Roentgenology 2014. ; 202 : 1366 – 75 . doi: 10.2214/AJR.13.12023 [DOI] [PubMed] [Google Scholar]
  • 16. Foti PV , Attinà G , Spadola S , Caltabiano R , Farina R , Palmucci S , et al. . MR imaging of ovarian masses: classification and differential diagnosis . Insights Imaging 2016. ; 7 : 21 – 41 . doi: 10.1007/s13244-015-0455-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Brown DL , Dudiak KM , Laing FC . Adnexal masses: US characterization and reporting . Radiology 2010. ; 254 : 342 – 54 . doi: 10.1148/radiol.09090552 [DOI] [PubMed] [Google Scholar]
  • 18. Hickey M , Ballard K . Farquhar C.Endometriosis . BMJ 2014. ; 348 : 1752 . [DOI] [PubMed] [Google Scholar]
  • 19. Nnoaham K , Hummelshoj L , Webster P , D’Hooghe T , de CiccoNardone F , et al. . World Endometriosis Research Foundation Global Study of Women’s Health Consortium . Impact of endometriosis on quality of life and work productivity: a multi-centre study across 10 countries . FertilSteril 2011. ; 96 : 366 – 73 . [Google Scholar]
  • 20. Huang H , Li C , Zarogoulidis P , Darwiche K , Machairiotis N , Yang L , et al. . Endometriosis of the lung: report of a case and literature review . European Journal of Medical Research 2013. ; 18 : 13 . doi: 10.1186/2047-783X-18-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Neis KJ , Neis F . Chronic pelvic pain: cause, diagnosis and therapy from a gynaecologist's and an endoscopist's point of view . Gynecological Endocrinology 2009. ; 25 : 757 – 61 . doi: 10.3109/09513590903230366 [DOI] [PubMed] [Google Scholar]
  • 22. Fadhlaoui A , Bouquet de la Jolinière J , Endometriosis FA . And infertility: how and when to treat? Frontiers in Surgery 2014. ; 1 : 24 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Vercellini P , Viganò P , Somigliana E , Fedele L . Endometriosis: pathogenesis and treatment . Nat Rev Endocrinol 2014. ; 10 : 261 – 75 . doi: 10.1038/nrendo.2013.255 [DOI] [PubMed] [Google Scholar]
  • 24. Eisenberg VH , Weil C , Chodick G , Shalev V . Epidemiology of endometriosis: a large population-based database study from a healthcare provider with 2 million members . BJOG: Int J Obstet Gy 2018. ; 125 : 55 – 62 . doi: 10.1111/1471-0528.14711 [DOI] [PubMed] [Google Scholar]
  • 25. Abbas S , Ihle P , Köster I , Schubert I . Prevalence and incidence of diagnosed endometriosis and risk of endometriosis in patients with endometriosis-related symptoms: findings from a statutory health insurance-based cohort in Germany . European Journal of Obstetrics & Gynecology and Reproductive Biology 2012. ; 160 : 79 – 83 . doi: 10.1016/j.ejogrb.2011.09.041 [DOI] [PubMed] [Google Scholar]
  • 26. Johnson NP , Hummelshoj L , Adamson GD , Keckstein J , Taylor HS , Abrao MS , et al. . World endometriosis Society consensus on the classification of endometriosis . Hum Reprod 2017. ; 32 : 315 – 24 . doi: 10.1093/humrep/dew293 [DOI] [PubMed] [Google Scholar]
  • 27. Chapron C , Chopin N , Borghese B , Foulot H , Dousset B , Vacher-Lavenu MC , et al. . Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution . Hum Reprod 2006. ; 21 : 1839 – 45 . doi: 10.1093/humrep/del079 [DOI] [PubMed] [Google Scholar]
  • 28. Coutinho A , Bittencourt LK , Pires CE , Junqueira F , de Oliveira Lima CMA , Coutinho E , Lima CM , Domngues RC , et al. . MR imaging in deep pelvic endometriosis: a pictorial essay . RadioGraphics 2011. ; 31 : 549 – 67 . doi: 10.1148/rg.312105144 [DOI] [PubMed] [Google Scholar]
  • 29. Lasmar RB , Lasmar BP , Pillar C . Diagram to map the locations of endometriosis . International Journal of Gynecology & Obstetrics 2012. ; 118 : 42 – 6 . doi: 10.1016/j.ijgo.2012.02.010 [DOI] [PubMed] [Google Scholar]
  • 30. Piketty M , Chopin N , Dousset B , Millischer-Bellaische A-E , Roseau G , Leconte M , et al. . Preoperative work-up for patients with deeply infiltrating endometriosis: transvaginal ultrasonography must definitely be the first-line imaging examination . Human Reproduction 2009. ; 24 : 602 – 7 . doi: 10.1093/humrep/den405 [DOI] [PubMed] [Google Scholar]
  • 31. Koninckx PR , Ussia A , Adamayan L , Wattiez A , Donnez J , definition Deep endometriosis: . Diagnosis, and treatment . Fertility and Sterility 2012. ; 98 : 564 – 71 . [DOI] [PubMed] [Google Scholar]
  • 32. Chamié LP , Blasbalg R , Pereira RMA , Warmbrand G , Serafini PC . Findings of pelvic endometriosis at transvaginal us, MR imaging, and laparoscopy . RadioGraphics 2011. ; 31 : E77 – E100 . doi: 10.1148/rg.314105193 [DOI] [PubMed] [Google Scholar]
  • 33. Bazot M , Darai E , Hourani R , Thomassin I , Cortez A , Uzan S , et al. . Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease . Radiology 2004. ; 232 : 379 – 89 . doi: 10.1148/radiol.2322030762 [DOI] [PubMed] [Google Scholar]
  • 34. Bazot M , Bharwani N , Huchon C , Kinkel K , Cunha TM , Guerra A , et al. . European Society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis . European Radiology 2017. ; 27 : 2765 – 75 . doi: 10.1007/s00330-016-4673-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Manganaro L , Anastasi E , Vinci V , Saldari M , Bernando S , Sollazzo P , et al. . Endometriosis: 10 keys points for MRI . Journal of Endometriosis and Pelvic Pain Disorders 2015. ; 7 : 10 – 18 . [Google Scholar]
  • 36. Siegelman ES , Oliver ER . MR imaging of endometriosis: ten imaging pearls . RadioGraphics 2012. ; 32 : 1675 – 91 . doi: 10.1148/rg.326125518 [DOI] [PubMed] [Google Scholar]
  • 37. Woodward PJ , Sohaey R , Mezzetti TP . Endometriosis: Radiologic-Pathologic correlation . RadioGraphics 2001. ; 21 : 193 – 216 . doi: 10.1148/radiographics.21.1.g01ja14193 [DOI] [PubMed] [Google Scholar]
  • 38. Foti PV , Farina R , Palmucci S , Vizzini IAA , Libertini N , Coronella M , et al. . Endometriosis: clinical features, MR imaging findings and pathologic correlation . Insights Imaging 2018. ; 9 : 149 – 72 . doi: 10.1007/s13244-017-0591-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. Ghezzi F , Raio L , Cromi A , Duwe D , Beretta P , Buttarelli M , et al. . ?Kissing ovaries?: A sonographic sign of moderate to severe endometriosis . Fertility and Sterility 2005. ; 83 : 143 – 7 . doi: 10.1016/j.fertnstert.2004.05.094 [DOI] [PubMed] [Google Scholar]
  • 40. Dallaudière B , Salut C , Hummel V , Pouquet M , Piver P , Rouanet J-P , et al. . MRI atlas of ectopic endometriosis . Diagnostic and Interventional Imaging 2013. ; 94 : 263 – 80 . doi: 10.1016/j.diii.2012.10.020 [DOI] [PubMed] [Google Scholar]
  • 41. Kataoka ML , Togashi K , Yamaoka T , Koyama T , Ueda H , Kobayashi H , et al. . Posterior cul-de-sac obliteration associated with endometriosis: MR imaging evaluation . Radiology 2005. ; 234 : 815 – 23 . doi: 10.1148/radiol.2343031366 [DOI] [PubMed] [Google Scholar]
  • 42. Moawad NS , Guido R , Ramanathan R , Mansuria S , Lee T . Comparison of laparoscopic anterior discoid resection and laparoscopic low anterior resection of deep infiltrating rectosigmoid endometriosis . JSLS 2011. ; 15 : 331 – 8 . doi: 10.4293/108680811X13125733356431 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43. De Nardi P , Ferrrari S . Deep Pelvic Endometriosis: A Multidisciplinary Approach. Verlag . Italy: : The British Institute of Radiology. ; 2011. . [Google Scholar]
  • 44. Yoon JH , Choi D , Jang K-T , Kim CK , Kim H , Lee SJ , et al. . Deep rectosigmoid endometriosis: “mushroom cap” sign on T2-weighted MR imaging . Abdom Imaging 2010. ; 35 : 726 – 31 . doi: 10.1007/s00261-010-9643-3 [DOI] [PubMed] [Google Scholar]
  • 45. Menni M , Facchetti L , Cabassa P . Extragenital endometriosis: assessment with MR imaging . A pictorial review.Br J Radiol 2016. ; 89 : 20150672 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. Beaty SD . Silva AC,De PetrisG . Bladder Endometriosis: Ultrasound and MRI Findings Radiol Case Rep 2006. ; 1 : 92 – 5 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Novellas S , Chassang M , Bouaziz J , Delotte J , Toullalan O , Chevallier etP . Anterior pelvic endometriosis: MRI features . Abdom Imaging 2010. ; 35 : 742 – 9 . doi: 10.1007/s00261-010-9600-1 [DOI] [PubMed] [Google Scholar]
  • 48. Gui B , Valentini AL , Ninivaggi V , Micco M , Zecchi V , Grimaldi PP , et al. . Shining light in a dark landscape: MRI evaluation of unusual localization of endometriosis . Diagn Interv Radiol 2017. ; 23 : 272 – 81 . doi: 10.5152/dir.2017.16364 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Alborzi S , Rasekhi A , Shomali Z , Madadi G , Alborzi M , Kazemi M , et al. . Diagnostic accuracy of magnetic resonance imaging, transvaginal, and transrectal ultrasonography in deep infiltrating endometriosis . Medicine 2018. ; 97 : e9536 . doi: 10.1097/MD.0000000000009536 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50. Manfredi R , PozziMucelli R . MRI of the female and male pelvis . Switzerland: : The British Institute of Radiology. ; 2015. . [Google Scholar]
  • 51. Jha RC , Zanello PA , Ascher SM , Rajan S , Imaging D-W . Diffusion-weighted imaging (DWI) of adenomyosis and fibroids of the uterus . Abdom Imaging 2014. ; 39 : 562 – 9 . doi: 10.1007/s00261-014-0095-z [DOI] [PubMed] [Google Scholar]
  • 52. Kubik-Huch RA , Weston M , Nougaret S , Leonhardt H , Thomassin-Naggara I , Horta M , et al. . European Society of urogenital radiology (ESUR) guidelines: MR imaging of leiomyomas . European Radiology 2018. ; 28 : 3125 – 37 . doi: 10.1007/s00330-017-5157-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53. Rauch GM , Kaur H , Choi H , Ernst RD , Klopp AH , Boonsirikamchai P , et al. . Optimization of MR imaging for pretreatment evaluation of patients with endometrial and cervical cancer . Radiographics 2014. ; 34 : 1082 – 98 . doi: 10.1148/rg.344140001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54. Balleyguier C , Sala E , Da Cunha T , Bergman A , Brkljacic B , Danza F , et al. . Staging of uterine cervical cancer with MRI: guidelines of the European Society of urogenital radiology . Eur Radiol 2011. ; 21 : 1102 – 10 . doi: 10.1007/s00330-010-1998-x [DOI] [PubMed] [Google Scholar]
  • 55. Lin Y , Li H , Chen Z , Ni P , Zhong Q , Huang H , et al. . Correlation of histogram analysis of apparent diffusion coefficient with uterine cervical pathologic finding . American Journal of Roentgenology 2015. ; 204 : 1125 – 31 . doi: 10.2214/AJR.14.13350 [DOI] [PubMed] [Google Scholar]
  • 56. Bourgioti C , Chatoupis K , Moulopoulos LA . Current imaging strategies for the evaluation of uterine cervical cancer . WJR 2016. ; 8 : 342 – 54 . doi: 10.4329/wjr.v8.i4.342 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57. National cancer Institute Cancer STAT fact sheets: sorpus and Uterus, NOS . Bethesda, Md. National Cancer Institute 2010. ;. [Google Scholar]
  • 58. Nougaret S , Horta M , Sala E , Lakhman Y , Thomassin-Naggara I , Kido A , et al. . Endometrial cancer MRI staging: updated guidelines of the European Society of urogenital radiology . Eur Radiol 2018. ;. [DOI] [PubMed] [Google Scholar]
  • 59. Kinkel K , Forstner R , Danza FM , Oleaga L , Cunha TM , Bergman A , et al. . Staging of endometrial cancer with MRI: guidelines of the European Society of urogenital imaging . Eur Radiol 2009. ; 19 : 1565 – 74 . doi: 10.1007/s00330-009-1309-6 [DOI] [PubMed] [Google Scholar]
  • 60. Fujii S , Kido A , Mikami Y , Matsumura N , Konishi I , Togashi K . Peritumoral enhancement in endometrial cancer on dynamic contrast-enhanced imaging: Radiologic-pathologic correlation . J Obstet Gynaecol Res 2014. ; 40 : 1445 – 9 . doi: 10.1111/jog.12318 [DOI] [PubMed] [Google Scholar]
  • 61. Bonatti M , Stuefer J , Oberhofer N , Negri G , Tagliaferri T , Schifferle G , et al. . MRI for local staging of endometrial carcinoma: is endovenous contrast medium administration still needed? European Journal of Radiology 2015. ; 84 : 208 – 14 . doi: 10.1016/j.ejrad.2014.11.010 [DOI] [PubMed] [Google Scholar]
  • 62. Lin G , Ng K-K , Chang C-J , Wang J-J , Ho K-C , Yen T-C , KK N , et al. . Myometrial invasion in endometrial cancer: diagnostic accuracy of diffusion-weighted 3.0-T Mr Imaging—Initial experience . Radiology 2009. ; 250 : 784 – 92 . doi: 10.1148/radiol.2503080874 [DOI] [PubMed] [Google Scholar]
  • 63. Das SK , Niu XK , Wang JL , Zeng LC , Wang WX , Bhetuwal A , et al. . Usefulness of DWI in preoperative assessment of deep myometrial invasion in patients with endometrial carcinoma: a systematic review and meta-analysis . Cancer Imaging 2014. ; 14 : 32 . doi: 10.1186/s40644-014-0032-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64. Luomaranta A , Leminen A , Loukovaara M , et al. . Magnetic resonance imaging in the assessment of high-risk features of endometrial carcinoma . International Journal of Gynecological Cancer 2015. ; 25 : 837 – 42 . doi: 10.1097/IGC.0000000000000194 [DOI] [PubMed] [Google Scholar]
  • 65. Sala E , Rockall AG , Freeman SJ , Mitchell DG , Reinhold C . The added role of MR imaging in treatment stratification of patients with gynecologic malignancies: what the radiologist needs to know . Radiology 2013. ; 266 : 717 – 40 . doi: 10.1148/radiol.12120315 [DOI] [PubMed] [Google Scholar]
  • 66. D'Angelo E , Prat J . Uterine sarcomas: a review . Gynecologic Oncology 2010. ; 116 : 131 – 9 . doi: 10.1016/j.ygyno.2009.09.023 [DOI] [PubMed] [Google Scholar]
  • 67. Bolan C , Caserta MP . MR imaging of atypical fibroids . Abdom Radiol 2016. ; 41 : 2332 – 49 . doi: 10.1007/s00261-016-0935-0 [DOI] [PubMed] [Google Scholar]

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