|Year : 2016 | Volume
| Issue : 2 | Page : 39-52
Imaging modalities in the differentiation of various adnexal lesions
Faten M Salem1, Reda A Alarabawy MD 1, Mona T El-Ebiary2, Ayman A Edorf2, Samar M Abozeid3
1 Department of Radiodiagnosis and Medical Imaging, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Department of Obstetrics and Gynecology, Faculty of Medicine, Tanta University, Tanta, Egypt
3 Department of Radiodiagnosis and Medical Imaging, El Menshawy General Hospital, Tanta, Egypt
|Date of Submission||10-Jan-2016|
|Date of Acceptance||15-Mar-2016|
|Date of Web Publication||29-Aug-2016|
Reda A Alarabawy
Department of Radiodiagnosis and Medical Imaging, Faculty of Medicine, Tanta University, Tanta
The purpose of this study was to discuss the role of different imaging modalities in the diagnosis and evaluation of adnexal masses.
Patients and methods
A total of 50 female patients with 60 adnexal lesions were included in his study. After clinical evaluation, ultrasound examination was carried out for all cases. After observing all gray scale features, color Doppler was superimposed on the gray images to assess the site of blood flow and measure the Doppler indexes. Computed tomography was performed in seven suspicious cases, and MRI was performed in eight suspicious cases. The results were correlated with operative and histopathological findings.
Nine malignant cases had Alcázar score greater than 6, whereas the benign cases (41 cases) had a score less than 6. There were two cases (4%) of hydrosalpinx, five cases (10%) of ectopic pregnancy, three cases (6%) of tuboovarian abscess, four cases (8%) of polycystic ovaries, and four cases of solid masses (8%) (one case of ovarian fibroma, one case of subserous uterine fibroid, one case of broad ligament fibroid, and one case of Krukenberg tumor). There were 24 cases of cystic masses (48%) either unilocular or multilocular within thin septae (seven cases of follicular ovarian cysts, eight cases of hemorrhagic cysts, one case of corpus luteal cyst, two cases of endometrioma, three cases of dermoid cysts, two cases of serous cystadenoma, and one case of paraovarian cyst). There were eight complex masses (16%) (one case of granulosa cell tumor, one case of dysgerminoma, one case of papillary carcinoma, one case of metastasis, two cases of serous cystadenocarcinoma, and two cases of mucinous cystadenocarcinoma).
Using ultrasound and color Doppler studies with scoring system was found to be useful in differentiating a benign from a malignant adnexal mass. Computed tomography scan has shown to be beneficial in assessing the disease extent and planning for treatment. MRI was beneficial in characterizing adnexal masses in problematic cases.
Keywords: adnexal lesion, differentiation, imaging modalities
|How to cite this article:|
Salem FM, Alarabawy RA, El-Ebiary MT, Edorf AA, Abozeid SM. Imaging modalities in the differentiation of various adnexal lesions. Tanta Med J 2016;44:39-52
|How to cite this URL:|
Salem FM, Alarabawy RA, El-Ebiary MT, Edorf AA, Abozeid SM. Imaging modalities in the differentiation of various adnexal lesions. Tanta Med J [serial online] 2016 [cited 2019 Mar 20];44:39-52. Available from: http://www.tdj.eg.net/text.asp?2016/44/2/39/189343
| Introduction|| |
The upper female genital tract consists of the uterus and the cervix with associated uterine (Fallopian) tubes and ovaries .
The term adnexa refers to the area of the Fallopian tube More Detailss and ovaries. Therefore, an adnexal mass is usually a mass involving the ovary or tube .
Adnexal masses, both painful and asymptomatic, are commonly encountered entities in clinical practice. Ultrasound (US) is usually the initial imaging investigation due to its wide availability, relatively low cost, portability, and lack of ionizing radiation. The goal is to identify distinguishing features of the adnexal mass and to assess its malignant potential. In some cases, follow-up US, computed tomography (CT), or MRI may be necessary .
The benefit of US is the characterization of an adnexal mass, suggesting the probable etiology of the mass. Masses may be divided as solid, cystic, or complex. It is predominantly the solid and complex masses that need a thorough evaluation. The role of color flow imaging is now gaining importance, and criteria for distinguishing between benign and malignant masses are often possible based on the principle that neovascularization occurs in malignant tumors and results in lower resistive index (RI < 0.4) and pulsatile index (PI < 1.0) ,. Availability of a scoring system enables the differentiation of small adnexal masses. Several benign lesions may present as complex masses but can be distinguished and diagnosed on sonography. Transvaginal sonography remains the investigation most commonly performed first for the investigation of ovaries, as it allows a more detailed assessment of morphologic features of an adnexal mass .
MRI is used to visualize internal structures of the body in detail using nuclear magnetic resonance to image the nuclei of atoms inside the body. Imaging of the indeterminate adnexal mass is now the most common indication for MRI. A sonographically indeterminate adnexal mass is defined as follow:
- One that has complexity that cannot be confidently placed into either the benign or malignant category or
- One for which the site of origin, from the ovary, uterus, or another pelvic structure remains to be established .
CT has been used to rule out metastatic disease. CT is carried out after US features suggest malignancy, such as solid component (particularly if there is visible flow in it at Doppler evaluation), thick septa (2–3 mm), bilaterality, and ascites . CT is useful for further workup and to define the extent of disease. CT is the preferred technique in the pretreatment evaluation of ovarian cancer to define the extent of disease (staging). Moreover, it may be useful for suspected malignancy on nonpelvic source and for evaluating tuboovarian abscesses by visualizing inflammatory changes .
The aim of our study was to evaluate the role of different imaging modalities in the characterization and differentiation of adnexal lesions.
| Patients and methods|| |
This retrospective study was performed during the period from October 2013 to July 2015 on consecutive 50 female patients referred from the Gynecology Department to the Radiology Department of Tanta University Hospital.
This study was conducted according to the guidelines of the ethics committee of our university and was approved by our institutional review board. All patients provided written informed consent to be imaged in our study.
History of recurrent lower abdominal pain, abdominal enlargement, bleeding per vagina, menstrual irregularity, or infertility.
All patients proved to have adnexal mass with diameter more than 3 cm.
Allergy from intravenous contrast media or renal insufficiency for patients who need CT with contrast.
Claustrophobic patients or those with any ferromagnetic material in their bodies or cardiac pacemakers when MRI is needed.
All patients included in the study were subjected to the following:
Gynecological and obstetric history taking.
General, abdominal, and pelvic examination.
Laboratory examination: complete blood picture, random blood sugar, erythrocyte sedimentation rate, C-reactive protein, pregnancy test, and tumor marker.
Transabdominal ultrasound examination (performed for all patients)
Abdominopelvic US was performed using a gray scale US machine (Toshiba, Nemio XG, Japan) with 3.5 MHz convex probe. The patients were asked to have full bladder as it displaces bowel and becomes an acoustic window to view the uterus and adnexal areas. The patients were made to lie in the supine position and examined in both longitudinal and transverse planes of the uterus and adnexa. This examination was practically valuable in patients with large pelviabdominal masses that were out of the limited field of view of transvaginal probe and in virgins.
Transvaginal ultrasound examination (carried out for selected patients)
Transvaginal ultrasound (TVUS) was performed using an US machine with 6 MHz transvaginal probe. The patients were asked to evacuate the bladder. The end of the probe was covered with gel, inserted into a condom, and finally recoated with gel and then gently inserted into the vagina. The patients were made to lie in the dorsal position. The probe was rotated side by side for better visualization of the uterus and ovaries (transverse scan and longitudinal scan). Color imaging may be used to identify vascular structures from the ovary. Measurement of the Doppler indexes was taken from the intraovarian arteries.
Morphological features of adnexal mass were assessed using a gray scale US on the basis of the following characteristics:
Unilateral or bilateral and maximum dimensions.
Nature of the mass: cystic, partially cystic, or entirely solid.
Outer wall structure: regular or irregular; inner wall structure: smooth or presence of papillary projections.
The echogenicity of the lesion: translucent, low, hyper, or mixed.
Presence of ascites.
The adnexal lesions encountered in this study were evaluated using US according to the scoring system of Alcázar (2003) , in which a score of 6 or greater was given to malignant lesions [Table 1].
Color Doppler examination (carried out for all patients)
Color Doppler examination was carried out using the same equipments and transducers.
Color flow map: After careful examination of the lesion using a gray scale real-time US, the color box was superimposed on the lesion site, surveying it entirely for feeding blood vessels (areas from which color signals were received).
Wave analysis: After identification of the feeding blood vessels of the lesion under examination, the pulsed wave Doppler sample was placed inside the vessel, which had been chosen until an appropriate arterial wave was obtained. Thereafter, the RI and the PI were calculated in selected cases.
Color Doppler parameters were optimized for the detection of slow or little flow as follows:
Color box size was kept small to cover only the area of interest.
The velocity scale was adjusted for the lowest flow possible.
The color wall filter was set to a minimum, 50–60 Hz.
The color gain was increased to the maximum and then reduced gradually until the disappearance of the background noise.
The gate size was usually two-third of the examined vessel lumen.
The Doppler angle is the most important parameter because the velocity measurement of the spectrum is dependent on the angle. The Doppler angle in our study was kept parallel to the lumen of the vessel and kept less than 60°.
Color Doppler imaging was assessed as follows: the presence or absence of vascularity, and the location of blood vessels, ‘peripheral or central’. Arterial flow was characterized by a biphasic flow velocity waveform with a systolic and a diastolic component, whereas venous flow was characterized by a monophasic continuous flow and calculation of the RI and the PI, which was used to estimate the arterial signals blood flow impedance.
Computed tomography examination (carried out for selected patients)
All CT examinations were performed on a (Toshiba Aquillion multislice 320; Toshiba) CT scanner. Patients lie in the supine position, and scans from the diaphragm to ischial tuberosities were obtained.
Patients were asked to fast for 5 h, with oral administration of contrast material (oral gastrografin: 1000 ml of a 2.5% solution). All scans were obtained spirally after intravenous administration of contrast material (60 ml of Ultravest contrast material at a rate of 3 ml/s) with slices of 3 mm thickness.
CT images were evaluated as follows: the appearance of the lesion, whether cystic, solid, or mixed with its maximum diameter; bilaterality; multilocularity; the cyst density on the noncontrast scans; cyst wall enhancement, the maximum thickness of the cyst wall; discontinuity or disruption of the cyst wall, extravasations of intravenous contrast media; the extent of ascites; loculated ascites; and the presence of peritoneal infiltrations.
MRI examination (carried out for selected patients)
MRI was performed on a (Toshiba Vintage 1.5-T; Toshiba) MRI unit. All patients were imaged in the supine position using pelvic phased-array coil to improve the image quality.
Patient preparation: Patients were asked to fast for at least 5 h before MRI. The sequences used in this study were as follows: axial T1 and with contrast (TR = 500 ms, TE = 10 ms, FOV = 380 mm, slice thickness = 6 mm); axial T2 and sagittal T2 and coronal T2 (TR = 4000 ms, TE = 90 ms, FOV = 400 mm, slice thickness = 7 mm); and coronal T1 fat suppressed (TR = 2200 ms, TE = 45 ms, FOV = 400 mm, slice thickness = 7 mm).
Postcontrast images were obtained after intravenous injection of gadolinium at a dose of 0.1 mmol/kg of body weight that were used for the recognition of enhancement of the solid component, the tumor wall, septations, and vegetations.
MRI were evaluated as follows: MR appearance of the tumor, whether cystic, solid, or mixed; involvement of one or both ovaries; signal intensity (SI) of the tumor; enhancement of the solid component if present; wall thickness of the tumor and its enhancement; presence of vegetations with their enhancement pattern and size; presence of ascites; presence of infiltrated pelvic or para-aortic lymph nodes; involvement of other pelvic organs; and presence of peritoneal or omental deposits.
Patients with polycystic ovary complaining of unstimulated cycles who had undergone laboratory tests revealed elevated luteinizing hormone and testosterone with normal or decreased follicle-stimulating hormone.
Patients with unilateral hydrosalpinx underwent hysterosalpingography for confirmation.
Final diagnosis was confirmed by means of surgery either laparoscope or open surgery and histopathologic confirmation in operated patients; other patients were followed up after 6 months.
| Results|| |
Transabdominal US and TVUS examinations of 50 patients revealed 60 adnexal lesions, 10 cases being bilateral.
The frequency of different complaints in the studied patients with different adnexal lesions shown in [Figure 1].
|Figure 1 Transvaginal ultrasonography (a) Revealing a right ovarian thin-walled anechoic simple cyst, measuring about 5.8 × 4.5 cm, with no solid parts or internal echoes. Color Doppler study (b) Revealing peripheral flow. Radiological diagnosis: a benign-looking right ovarian simple cyst.|
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The patients presented clinically with different complaints: half of the studied cases (25 cases) complained of abdominal pain (50%), and abdominal pain associated with abdominal enlargement was observed in 14 cases (28%). Other complaints (nine cases) (18%) were menstrual abnormalities (four cases), vaginal bleeding (three cases), and infertility (two cases). Two cases (4%) were accidentally discovered as adnexal mass during US examination.
The age of the patients with benign masses ranged between 20 and 50 years, and in cases of malignant masses the age ranged between 37 and 64 years.
Relationship of benign and malignant masses with period of life is shown in [Figure 2].
|Figure 2 Transvaginal ultrasonography (a) Revealing left ovarian echogenic cystic lesion with low level of internal echoes seen inside, measuring 4.2 × 3.6 cm at maximum dimensions. Color Doppler study (b) Revealing minimal peripheral flow. Radiological diagnosis: left ovarian endometrioma (chocolate cyst).|
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Benign lesions were founded in 50% of patients in the reproductive period and in 22% of patients in the premenopausal period, and in five patients (10%) in the postmenopausal period, whereas malignant lesions were founded in two cases (4%) in the premenopausal period and in seven cases (14%) in the postmenopausal period.
The percentage of different modalities used in our study was as follows:
US (abdominal and transvaginal) was performed in all cases (100%).
Pulsed Doppler was performed in 17 cases (34%).
MRI was performed in eight cases (16%).
CT was performed in seven cases (14%).
The diagnosis was confirmed by means of histopathology in 15 operated cases (30%).
According to the scoring system of Alcázar (2003)(9) [Table 2], the malignant cases (nine) had a score greater than 6 (ranging from 8 to 10) due to the presence of solid areas or purely solid echogenicity and central blood flow with low resistance, whereas the benign cases (41) had a score less than 6 (ranging from 0 to 4) due to the absence of thick papillary projection, peripheral or absence of blood flow within the lesions with the presence of solid areas, or purely solid echogenicity only in 16 cases [Table 3].
|Table 2 Classification and scoring of the studied cases by means of ultrasound according to the scoring system proposed by Alcázar (2003) |
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On gray scale US, the 50 studied cases included the following [Figure 3]:
|Figure 3 Abdominal ultrasonography (a) Revealing an ovoid-shaped right adnexal isoechoic mass, measuring about 13 × 8 cm, which is seen separable from the uterus (U). Color Doppler study (b) Revealing peripheral flow. Pulsed Doppler study (c) Revealing minimal flow with pulsatile index (PI) = 1 and resistive index (RI) = 0.7. Radiological diagnosis: a broad ligament fibroid.|
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Two cases (4%) of hydrosalpinx (oblong-shaped tubal clear cystic lesions).
Five cases (10%) of ectopic pregnancy (tubal hematoma, blood in pelvis, empty uterus, positive pregnancy test, and tender transvaginal probe).
Three cases (6%) of tuboovarian abscess (oblong-shaped tubal cystic lesion with internal echoes).
Four cases (8%) of polycystic ovaries (both enlarged ovaries show peripheral subcentemetric follicles).
Four solid masses (8%) (one case of ovarian fibroma, one case of subserous uterine fibroid, one case of broad ligament fibroid, and one case of Krukenberg tumor).
Twenty-four cystic masses (48%) either unilocular or multilocular within thin septae (seven cases of follicular ovarian cysts, eight cases of hemorrhagic cysts, one case of corpus luteal cyst, two cases of endometrioma, three cases of dermoid cysts, two cases of serous cystadenoma, and one case of paraovarian cyst).
Eight complex masses (16%) either predominantly cystic masses or predominantly solid masses (one case of granulosa cell tumor, one case of dysgerminoma, one case of papillary carcinoma, one case of metastasis, two cases of serous cystadenocarcinoma, and two cases of mucinous cystadenocarcinoma).
Pulsed Doppler study was carried out in eight benign cases and nine malignant cases ([Table 4], [Figure 4],[Figure 5]).
|Table 4 The pulsatility and resistive indexes of the studied cases using power Doppler study|
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|Figure 4 Abdominal ultrasonography (a) Revealing right multilocular anechoic cystic lesion, measuring about 12 × 10 cm at its maximum dimensions with thin septae; no solid parts. Color Doppler study (b) Revealing peripheral flow and minimal flow in the septae. Pulsed Doppler study (c) Revealing arterial flow with pulsatile index (PI) = 0.9 and resistive index (RI) = 0.6. Postcontrast computed tomography (CT) scan (d) Revealing a multilocular thin-septated right adnexal cystic lesion with homogenous attenuation, measuring about 13 × 10.5 cm. Radiological diagnosis: benign-looking right ovarian cyst, likely to be a serous cystadenoma.|
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|Figure 5 Abdominal ultrasonography (a) Revealing right multilocular cystic lesion with solid component, measuring about 7.3 × 5.6 cm at its maximum dimensions. Color and pulsed Doppler study (b) Revealing peripheral and central blood flow. The arterial flow with pulsatile index (PI) = 0.8 and resistive index (RI) = 0.4. Postcontrast computed tomography (CT) scan (c) Revealing a right complex multilocular adnexal cystic lesion of different attenuation and enhancing septae, measuring about 6.5 × 5 cm. Radiological diagnosis: a malignant-looking right ovarian complex lesion, likely to be a mucinous cystadenocarcinoma, and this was confirmed by pathology.|
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In the eight benign cases, the RI was 0.6 ± 0.1 and PI measured was 1.0 ± 0.3 (about seven cases showed PI more than 0.1 and RI more than 0.4, and one case showed PI less than 0.1 and RI less than 0.4).
In the nine malignant cases, the RI measured was 0.4 ± 0.1 and PI measured was 0.7 ± 0.4 (seven cases of the nine malignant lesions had PI less than 0.1 and RI less than 0.4, and the remaining two cases had PI more than 0.1 and RI more than 0.4).
Overall the PI and RI indexes tend to be lower in malignant than in benign lesions.
On CT examination, seven lesions were diagnosed on complementary CT scan as benign or malignant tumors, and the results were confirmed by pathology, which is considered the main reference [Table 5].
Postcontrast CT scan was performed in seven cases (one case of corpus luteal cyst, one case of ovarian fibroma, one case of serous cystadenoma, one case of serous cystadenocarcinoma, one case of mucinous cystadenocarcinoma, one case of granulosa cell tumor, and one case of papillary carcinoma). Pelvic ascites and omental cakes were detected in one case of papillary carcinoma.
On MRI examination, eight lesions were diagnosed on conventional MRI as benign or malignant tumors, and the results were confirmed by pathology, which is considered the main reference [Table 6].
Conventional MRI was performed in eight cases (two cases of hemorrhagic cysts, one case of dermoid cyst, one case of endometrioma, one case of tuboovarian abscess, one case of hydrosalpinx, one case of dysgerminoma, and one case of Krukenberg tumor). Pelvic ascites was detected in one case of Krukenberg tumor. Postcontrast enhancement was detected in two cases (dysgerminoma and Krukenberg tumor).
The diagnosis was confirmed by means of histopathological examination of the 15 operated cases [Table 7].
| Discussion|| |
The accurate diagnosis of an adnexal mass as benign or malignant is crucial to avoid unnecessary radical surgery, especially in postmenopausal women, and can help young women wishing to preserve childbearing potential to opt conservative surgery .
Proper management depends on proper preoperative assessment with the help of clinical examination, laboratory tests, and different imaging modalities, thus helping in informing the patient about the surgical route and the feasibility of conservative treatment .
Pelvic US, Doppler study, MRI, and CT are more common modalities in the assessment of adnexal swelling.
In the current study, 50 patients with adnexal lesions were included. The aim of the current study was to evaluate the abilities of US (abdominal and vaginal) and color Doppler for better characterization of adnexal lesions. Complementary CT scan was performed in seven cases and conventional MRI was performed in eight cases.
In the present study, the probability of malignancy increased with age (mean age 29.3 years in benign masses and 46 years in malignant masses). These results coincide with those of Brown et al. (1998) , who analyzed the relationship between malignancy, age, and menopausal state. They showed that, with older age, the probability of malignancy increases (mean age was 38.8 ± 12 years in benign cases vs. 48 ± 15.4 years in malignant cases).
Analysis of the ultrasound morphological study of the adnexal masses
In this study, seven cases of functional ovarian cysts appeared as well-defined, thin-walled, echo-free cysts. This is in agreement with the findings of Valentin (2004) , who considered unilocular and multilocular cysts without solid components to be benign.
In the current study, eight cases of hemorrhagic ovarian cysts presented as well-defined, unilocular, thin-walled cyst with multiple nonvascular fine strands in six cases and nonvascular clot in two cases. Two cases with endometrioma appeared as diffuse homogenously low-level echoes within well-marginated thin-walled cysts. No solid parts were detected.
Three cases with dermoid cysts had a densely echogenic mural tubercle with posterior acoustic shadow within a cystic component. This coincides with findings of Guerriero et al. (2005) , who found that it is characterized by one of the following three echopatterns:
- A densely echogenic mural tubercle with posterior acoustic shadow associated with a cystic echopattern;
- Echogenic thin band-like echoes (hyperechoic lines and dots in dark field); and
- A dense echopattern associated with posterior acoustic shadow with or without a cystic component.
In our study, thick septa was found in one benign case (serous cystadenoma) and it was not found in the two malignant cases (serous cystadenocarcinoma and mucinous cystadenocarcinoma). The presence of solid component and mixed echogenicity was the criteria of the two malignant cases, and this is in agreement with the findings of Alcázar et al. (2003) , who found that thick septae were not correlated with malignancy (their study included 705 adnexal masses in 665 patients). They found that the only morphologic parameters that were associated independently with malignancy were thick papillary projections and solid areas.
In this study, two cases of serous cystadenoma were seen as multilocular cysts of thin regular walls, one of them with thin septae (<3 mm) and the other case with thick septae (>3 mm) with no papillary projections. However, it was considered benign according to the Alcázar scoring system. This is in agreement with findings of Guerriero et al. (2005) .
In the present study, the three cases with tuboovarian abscesses complained of pelviabdominal pain, and the ipsilateral adnexal region was tender on examination. On US examination, they appeared as a complex structure with thick walls and thick septae, filled with turbid material.
In the present study, five cases with ectopic pregnancy complained of abdominal pain after a period of amenorrhea. There was an empty uterus on transabdominal US. On TVUS, ectopic pregnancy was suspected by the presence of juxtaovarian complex adnexal mass. Color Doppler demonstrated surrounding hyperemia in which viability of fetal node was demonstrated in one case. This is in agreement with the findings of Fleischer and Entman (2001) , who stated that the diagnosis of ectopic pregnancy is often suggested in women who presented with lower abdominal pain and a period of amenorrhea. The use of TVUS has greatly enhanced the sonographic evaluation of patients with suspected ectopic pregnancy, specifically to document the presence or absence of an intrauterine gestation. In addition, adnexal masses created by ectopic pregnancies can be more frequently detected on TVUS. Moreover, it can demonstrate extrauterine gestational sac, corpus luteum cyst, or both. Viable trophoblastic tissue produces a vascular ring within the tube that can be recognized by means of color Doppler study.
In the current study, two cases with hydrosalpinx were seen as a fluid-filled sausage-shaped cystic structure with the presence of incomplete septae. This is in agreement with the findings of Valentin (2004) .
In our study, one case of paraovarian cyst was detected as a well-defined, thin-walled, echo-free cyst, which is seen separable from the ipsilateral ovary. One case of broad ligament fibroid was diagnosed as a well-defined solid lesion, isoechoic to the myometrium that was seen separable from the uterus and either ovary. All three cases of juxtauterine extraovarian masses (broad ligament fibroid, paraovarian cyst, and subserous fibroid) were separable from the normal ovary. These findings are in agreement with the statements of Madan (2006) , who reported that the differentiation of juxtauterine masses (subserosal myomas, adnexal masses, bowel masses, and other pelvic lesions) depends on the imaging characteristics of the mass, such as its content and architecture, and the relation of the uterine serosa to the mass. Moreover, a pelvic mass that is attached to the round ligament of the uterus has a high probability to be a uterine leiomyoma rather than an adnexal mass. The presence or absence of normal visible ovaries is one of the useful clues in assessing the origin of a pelvic mass.
Angiogenesis is an essential event in malignant tumor growth in which new vessels are formed within the tumor. These vascular changes can be detected by means of color Doppler study. Transvaginal color Doppler assessment of adnexal masses was used in an attempt to improve the diagnostic accuracy of gray scale US in determining the nature (benign or malignant). This technique was based on the fact that Doppler allows the assessment of angiogenesis in vivo .
The introduction of color Doppler scanning allowed the assessment of tumor vascularity. Its addition decreases the false-positive rate of morphologic evaluation .
In the present study, the 16 cases of ovarian cysts (seven functional, eight hemorrhagic, and one corpus luteal cysts) showed minimal peripheral flow in 13 cases, and no flow was detected in three cases (two functional and one hemorrhagic cysts). This is in agreement with the findings of Guerriero et al. (2002) , who found that the risk for malignancy associated with unilocular echo-free cysts is very low. In these masses, Doppler sonography does not improve diagnostic accuracy. In contrast, complex adnexal cysts shown on sonography have a higher risk for malignancy.
In the present study, the two cases of endometrioma showing no color flow in their echogenic portions confirmed their cystic nature and it was valuable in excluding malignancy. The three cases of cystic teratoma were diagnosed as dermoid cyst, and showed typical sonographic appearance; peripheral flow was detected only in one case, whereas no flow was detected in the other two cases. This is in agreement with the findings of Timor-Tritsch et al. (1998) , who stated that the absence of color flow in different echogenic portions as in dermoid plug and clots in hemorrhagic cysts and in endometrioma were helpful in identifying their cystic nature.
The use of color Doppler to increase the specificity of B-mode ultrasonography in the diagnosis of ovarian cancer is a safe diagnostic procedure with a very low risk of false-negative cases (104). In the present study, vessels were noted in the cyst wall in the benign cases, in contrast to malignant cases, showing peripheral and central vascularity in the solid parts. This is in agreement with the findings of Guerriero et al. (2005) , who considered masses with flow detected within the solid areas of very high risk for malignancy. This coincides with the findings of Fleischer et al. (1993)  as well, who found a significant difference between vascularization in benign lesions tending to be peripheral and vascularization in malignant lesions, which tend to be internal.
The use of Doppler indexes of tumor vascularity as markers of malignancy is a subject of debate. No standard has been established concerning the use of a certain Doppler index and cutoff value between benign and malignant masses . Stein et al. (1995)  suggested that spectral data obtained with RI and PI are not useful in differentiating benign from malignant masses and that both were significantly lower in malignant masses with too much overlap to be useful in individual cases.
In the present study, the RI measured in benign lesions was 0.6 ± 0.1 and that in malignant lesions was 0.4 ± 0.1. The PI measured in benign lesions was 1.0 ± 0.3 and that in malignant lesions was 0.7 ± 0.4. This agreed with Kurjak et al. (1992)  and Salem et al. (1994)  Who reported both high sensitivity and specificity in differentiating malignant from benign masses.
In our study, the spectral data obtained with RI and PI revealed some overlap noted between the reported values; this coincides with that reported by Fleischer et al. (1993) , who described some overlap in the values with several benign lesions having PI less than 1.0.
Role of computed tomography in diagnosing adnexal masses by assessing disease extent and planning treatment 
In the present study, the case of serous cystadenoma appeared as a thin-walled multilocular cystic lesion with homogenous attenuation and thin septations. This is in agreement with the findings of Jung et al. (2002) , who stated that benign serous cystadenoma appeared on CT as a unilocular or multilocular cystic mass with homogeneous attenuation of the locules with thin regular wall or septum and no endocystic or exocystic vegetation.
In the current study, the case of serous cystadenocarcinoma appeared as a multilocular cystic lesion of homogenous attenuation with thick septae and solid component. This is in agreement with the findings of Jeong et al. (2000) , who stated that malignant serous cystadenocarcinoma demonstrated solid components and multilocularity, having high attenuation on CT.
In the present study, two cases of mucinous cystadenocarcinoma appeared as multiple locules of different attenuation with solid component. This is agreement with the findings of Jung et al. (2002) , who stated that malignant mucinous cystadenocarcinoma manifested as a thick-walled multilocular cystic mass with papillary projection that contains liquids of different attenuation on CT.
In our study, the case of granulosa cell tumor appeared as a lobular complex (solid and cystic) lesion with different attenuation. This is in agreement with the findings of Wasnik et al. (2013) , who stated that granulosa cell tumor presented as a complex mass with solid and cystic component, sometimes showing a honeycomb pattern. The multilocular cystic spaces are usually filled with hemorrhage or serous fluid on CT.
In the present study, the case of papillary carcinoma had pelvic ascites and omental cakes with a complex (solid and cystic) ovarian lesion. This is agreement with the findings of Kim et al. (2004) , who stated that CT features of ovarian papillary carcinoma are mesenteric or omental involvement, ascites, peritoneal thickening, and normal appearing ovaries.
In our study, the case of ovarian fibroma appeared as a solid homogenous lesion. This is in agreement with the findings of Yen et al. (2013) , who stated that CT of ovarian fibroma appeared as a homogeneous solid tumor with delayed enhancement.
The current result of the case of corpus luteal cyst appeared as a unilocular cystic low-attenuated lesion with hyperattenuated wall. This is in agreement with the findings of Potter and Chandrasekhar (2008) , who stated that CT of corpus luteal cysts is often unilocular with thick high-attenuated walls. Wall enhancement is caused by the proliferation of blood vessels.
MRI has shown to be more specific and accurate compared with US and Doppler assessment in characterizing adnexal masses. In addition, it is the best method in the delineation of local spread to the pelvic organs .
In the present study, the two cases of hemorrhagic cysts displayed high signal on both T1WIs and T2WIs. This is in agreement with the findings of Wasnik et al. (2013) , who stated that MRI of hemorrhagic cysts shows a characteristic appearance of blood products manifested by relatively high SI on T1-weighted images and intermediate-to-high SI on T2-weighted images.
In the current study, the case of endometrioma displayed high signal on T1WIs and low signal on T2WIs. This is in agreement with the findings of Takeuchi et al. (2008) , who stated that hyperintense cyst on T1-weighted images that is hypointense on T2-weighted images (shading) are definite MRI signs of endometrioma.
In the present study, the case of dermoid cyst showed mixed SI: fat SI displaying high signals on T1WIs and T2WIs, with loss of bright SI in fat-suppressed sequence and areas of fluid signal displaying low SI on T1WIs and high SI on T2WIs. This is in agreement with the findings of Pereira et al. (2005) , who stated that mature cystic teratomas are usually unilocular. They are cystic tumors containing well-differentiated derivatives from at least two of the three germ cell layers (ectoderm, mesoderm, and endoderm). On T1WIs, it has high SI due to its fat content. On T2WIs, the SI is variable, usually is similar to that of fat. The SI in both T1 and T2WIs may mimic hemorrhagic lesions, mostly endometriomas. Frequency selective fat suppression technique is useful for differentiating these two common entities.
The current result of the case of tuboovarian abscess displayed low SI on T1WIs and intermediate-to-high SI on T2WIs. This is agreement with the findings of Kim et al. , who stated that MRI of tuboovarian abscess usually appeared as a pelvic mass with low SI on T1-weighted images and heterogeneous high SI on T2-weighted images. The SI of the content of the abscess can vary depending on its viscosity or protein concentration.
The current result of the case of hydrosalpinx displayed tubal clear cystic lesion with incomplete septa and had low SI on T1WIs and high SI on T2WIs. This is in agreement with the findings of Kim et al. (2009) , who stated that the MRI of the hydrosalpinx appeared as a fluid-filled tubular structure that arises from the upper lateral margin of the uterine fundus and was separate from the ipsilateral ovary. A dilated fallopian tube forms a sausage-like C-shaped or S-shaped cystic mass. The SI of the tubal fluid depends on the cause of the obstruction. On T1-weighted images, the SI of the content of a dilated fallopian tube usually is that of simple fluid (low SI on T1WIs and high SI on T2WIs), but the tubal content may have high SI if it is hemorrhagic or proteinaceous.
The current result of the case of dysgerminoma displayed intermediate SI on T1WIs and intermediate-to-high SI on T2WIs, with heterogeneous enhancement in postcontrast study (the diagnosis was confirmed by means of histopathological examination). This is contradictory to the findings of Lazebnik et al. (2009) , who stated that, on MRI, dysgerminoma has been described as having a multilobulated solid appearance with the lobules divided by fibrovascular septa.
In the present study, the case of Krukenberg tumor appeared as a bilateral complex lesion and displayed low SI on T1WIs and nonuniform high SI on T2WIs with pelvic ascites. This is in agreement with the findings of Jung et al. (2002) , who stated that Krukenberg tumor demonstrates some distinctive findings, including bilateral complex masses with hypointense solid components and internal hyperintensity on T1-weighted and T2-weighted MRI.
As regards the signal characteristics of adnexal masses studied in this work, cystic benign tumors showed low SI in T1WIs and high SI on T2WIs, and complex benign-looking masses showed high SI on T1WI and was considered as either fat or blood. On fat suppressed images low SI was noted with fat, whereas high SI was still noted in blood, and solid tumor showed low SI in T1WI and high SI on T2WI. Malignant criteria included the presence of wall thickness greater than 3 mm, solid vegetations more than 1 cm, thick septa more than 3 mm, and areas of necrosis and breaking down. Signs of tumor spread for staging were enlarged lymph nodes with lost fatty hilum, ascites, peritoneal, and omental deposits.
| Conclusion|| |
It is desirable to preoperatively differentiate benign, borderline ovarian tumors, and invasive ovarian cancers to decide whether surgery is required and which type of surgery is appropriate. Thus, it can help in avoiding unnecessary interference ([Figure 6], [Figure 7], [Figure 8] and [Diagram 1], [Diagram 2], [Diagram 3], [Diagram 4], [Diagram 5]).
|Figure 6 Abdominal ultrasonography (a) Revealing a large complex (solid and cystic) mass, measuring about 17.5 × 11 cm being inseparable from the left ovary. Color Doppler study (b) Revealing peripheral and randomly distributed central color flow. Postcontrast computed tomography (CT) scan (c, d) Revealing left-sided large lobular complex mass (solid and cystic), measuring about 18 × 11.5 cm, with irregular enhancement. Imaging-based diagnosis: a malignant-looking complex left ovarian mass. Pathological diagnosis: granulosa cell tumor (malignant sex cord stromal tumor).|
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|Figure 7 Transvaginal ultrasonography with color Doppler (a) Revealing a right well-defined thin-walled cyst with fine strands seen inside, measuring about 13.5 × 10.5 cm in its maximum dimensions, with peripheral color flow; no flow was detected in the internal strands. Conventional MRI examination (b, c) Revealing a large unilocular right adnexal lesion. It displayed high-signal intensity on T1WI (b), And also high-signal intensity on T2WI. (c). Radiological diagnosis: a benign-looking right hemorrhagic ovarian cyst.|
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|Figure 8 Transabdominal ultrasonography (a, b) Revealing bilateral complex (solid and cystic) adnexal lesions not separable from the uterus, measuring 13 × 10.5 cm at right and 9.5 × 7 cm at left. Color Doppler study (c) Revealing increased vascularity and peripheral and central color flow. Pulsed Doppler study (d) Revealing arterial flow with pulsatile index (PI) = 0.7 and resistive index (RI) = 0.4. Conventional MRI examination (e, f, g) Revealing bilateral, large, mixed adnexal lesions extending to the abdominal cavity and inseparable from the fundus and posterior wall of the uterus, measuring 14 × 11 × 10 cm at right and 10 × 7 × 5 cm at left. It displayed intermediate-signal intensity on T1WI and intermediate to-high-signal intensity on T2WI with heterogeneous enhancement in the postcontrast images. Imaging-based diagnosis: a malignant-looking bilateral complex ovarian lesions. Pathological diagnosis: dysgerminoma (malignant germ cell tumor).|
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US (abdominal and vaginal) is the primary modality for the detection of adnexal masses, being available and inexpensive.
The introduction of color Doppler scanning allowed the assessment of lesion vascularity and calculation of the RI and the PI and help in the assessment of the neoplastic nature of the lesions.
Using US and color Doppler studies with the use of a scoring system was found to be useful in differentiating a benign from a malignant adnexal mass.
CT scan provides cystic and solid component characterization based on different densities and plays a useful role in assessing the disease extent and planning for treatment.
Conventional MRI provides soft tissue characterization in problematic cases based on different SI and contrast uptake in postcontrast images.
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Conflicts of interest
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| References|| |
Hutson J. Development of the urogenital system. In: Standring S. editor Gray's anatomy
. 40th ed. Churchill Livingstone: Elsevier; 2008. 1305–1325.
Mann GS, Blair JC, Garden AS. Imaging of gynecological disorders in infants and children. Diagn Imag Tech 2012; 10:1007–1174.
DeLancey JOL. Principles of anatomy and perioperative considerations. In: Rock JA, Thompson JD, editors. TeLinde's Operative Gynecology. 8th ed. Philadelphia: Lippincott-Ravens; 1997. p. 77.
Theodoridis TD, Zepiridis L, Mikos T, Grimbizis GF, Dinas K, Athanasiadis A, Bontis JN. Comparison of diagnostic accuracy of transvaginal ultrasound with laparoscopy in the management of patientswith adnexal masses. Arch Gynecol Obstet 2009; 280:767–773.
Spencer JA, Ghattamaneni S. MR imaging of the sonographically indeterminate adnexal mass. Radiology 2010; 256:677–694.
Brown DL, Dudiak KM, Laing FC. Adnexal masses: US characterization and reporting. Radiology 2010; 254:342–354.
Drake J. Diagnosis and management of the adnexal mass. Am Fam Physician 1998; 57:2471–2476.
Alcázar JL, Mercé LT, Laparte C, Jurado M, López-García G. A new scoring system to differentiate benign from malignant adnexal masses. Am J Obstet Gynecol 2003; 188:685–692.
Kierans AS, Bennett GL, Mussi TC, Babb JS, Rusinek H, Melamed J, Rosenkrantz AB. Characterization of malignancy of adnexal lesions using ADC entropy: comparison with mean ADC and qualitative DWI assessment. J Magn Reson Imaging 2013; 37:164–171.
Thomassin-Naggara I, Toussaint I, Perrot N, Rouzier R, Cuenod CA, Bazot M, Daraï E. Characterization of complex adnexal masses: value of adding perfusion- and diffusion-weighted MR imaging to conventional MR imaging. Radiology 2011; 258:793–803.
Brown DL, Doubilet PM, Miller FH, Frates MC, Laing FC, DiSalvo DN, et al.
Benign and malignant ovarian masses: selection of the most discriminating gray-scale and Doppler sonographic features. Radiology 1998; 208:103–110.
Valentin L. Use of morphology to characterize and manage common adnexal masses. Best Pract Res Clin Obstet Gynaecol 2004; 18:71–89.
Guerriero S, Ajossa S, Garau N, Piras B, Paoletti AM, Melis GB. Ultrasonography and color Doppler-based triage for adnexal masses to provide the most appropriate surgical approach. Am J Obstet Gynecol 2005; 192:401–406.
Fleischer AC, Entman SS. Sonography evaluation of pelvic masses with transabdominal and/or transvaginal sonography. In: Fleischer AC, Manning FA, Jeanty P, Romero R, editors. Sonography in obstetrics and gynecology: principles and practice. 6th ed. New York (NY): McGraw-Hill; 2001. p. 883–911.
Madan R. The bridging vascular sign. Radiology 2006; 238:371–372.
Alcázar JL, López-García G. Transvaginal color Doppler assessment of venous flow in adnexal masses. Ultrasound Obstet Gynecol 2001; 17:434–438.
Guerriero S, Alcazar JL, Coccia ME, Ajossa S, Scarselli G, Boi M, et al.
Complex pelvic mass as a target of evaluation of vessel distribution by color Doppler sonography for thediagnosis of adnexal malignancies: results of a multicenter European study. J Ultrasound Med 2002; 21:1105–1111.
Timor-Tritsch IE, Lerner JP, Monteagudo A, Murphy KE, Heller DS. Transvaginal sonographic markers of tubal inflammatory disease. Ultrasound Obstet Gynecol 1998; 12:56–66.
Fleischer AC, Kepple DM, Entman SS. Transvaginal sonography of uterine disorders In: Timor-Tritsch IE, Rottem S, editors. Transvaginal sonography. 2nd ed. New York: Elsevier Science Publishing; 1991. 109–130.
Reles A, Wein U, Lichtenegger W. Transvaginal color Doppler sonography and conventional sonography in the preoperative assessment of adnexal masses. J Clin Ultrasound 1997; 25:217–225.
Stein SM, Laifer-Narin S, Johnson MB, Roman LD, Muderspach LI, Tyszka JM, Ralls PW. Differentiation of benign and malignant adnexal masses: relative value of gray-scale, color Doppler, and spectral Doppler sonography. Am J Roentgenol 1995; 164:381–386.
Kurjak A, Schulman H, Sosic A, Zalud I, Shalan H. Transvaginal ultrasound, color flow, and Doppler waveform of the postmenopausal adnexal mass. Obstet Gynecol 1992; 80:917–921.
Salem S, White LM, Lai J. Doppler sonography of adnexal masses: the predictive value of the pulsatility index in benign and malignant disease. Am J Roentgenol 1994; 163:1147–1150.
Jeong YY, Outwater EK, Kang HK. Imaging evaluation of ovarian masses. Radiographics 2000; 20:1445–1470.
Jung SE, Lee JM, Rha SE, Byun JY, Jung JI, Hahn ST. CT and MR imaging of ovarian tumors with emphasis on differential diagnosis. Radiographics 2002; 22:1305–1325.
Wasnik AP, Menias CO, Platt JF, Lalchandani UR, Bedi DG, Elsayes KM. Multimodality imaging of ovarian cystic lesions: review with an imaging based algorithmic approach. World J Radiol 2013; 5:113–125.
Kim HJ, Kim JK, Cho KS. CT features of serous surface papillary carcinoma of the ovary. Am J Roentgenol 2004; 183:1721–1724.
Yen P, Khong K, Lamba R, Corwin MT, Gerscovich EO. Ovarian fibromas and fibrothecomas: sonographic correlation with computed tomography and magneticresonance imaging: a 5-year single-institution experience. J Ultrasound Med 2013; 32:13–18.
Potter AW, Chandrasekhar CA. US and CT evaluation of acute pelvic pain of gynecologic origin in nonpregnant premenopausal patients. Radiographics 2008; 28:1645–1659.
Roach S, Hulse P, Carrington B. Ovarian Cancer. In: Hulse PA, Carrington BM, Carrington BM, editors. MRI manual of pelvic cancer. 2nd ed. London, UK: Taylor and Francis; 2004. 92–96.
Takeuchi M, Matsuzaki K, Nishitani H. Susceptibility-weighted MRI of endometrioma: preliminary results. Am J Roentgenol 2008; 191:1366–1370.
Pereira JM, Sirlin CB, Pinto PS, Casola G. CT and MR imaging of extrahepatic fatty masses of the abdomen and pelvis: techniques, diagnosis, differentialdiagnosis, and pitfalls. Radiographics 2005; 25:69–85.
Kim MY, Rha SE, Oh SN, Jung SE, Lee YJ, Kim YS, et al. MR Imaging findings of hydrosalpinx: a comprehensive review. Radiographics 2009; 29:495–507.
Lazebnik N, Balog A, Bennett S, Redline R, Liu J. Ovarian dysgerminoma: a challenging clinical and sonographic diagnosis. J Ultrasound Med 2009; 28:1409–1415.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]