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 Table of Contents  
Year : 2019  |  Volume : 32  |  Issue : 3  |  Page : 881-888

The role of diffusion-weighted MRI on the differentiation of complex adnexal masses

1 Department of Diagnostic Radiology, Faculty of Medicine, Menoufia University Hospital, Shebin El-Kom, Menoufia Governorate, Egypt
2 Department of Diagnostic Radiology, Bolaq El-Dakror Hospital, Bolaq El-Dakror, Giza Governorate, Egypt

Date of Submission25-Mar-2018
Date of Acceptance21-Apr-2018
Date of Web Publication17-Oct-2019

Correspondence Address:
Hamed G Ali
Shebin El-Kom 32511, Menoufia Governorate
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/mmj.mmj_100_18

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Conventional MRI has an established role in gynecologic imaging. However, increasing clinical demand for improved lesion characterization and disease mapping to optimize patient management has resulted in the incorporation of newer sequences, such as diffusion-weighted imaging (DWI), into routine protocols for pelvic MRI. DWI provides functional information on the microenvironment of water in tissues, hence augmenting the morphologic information derived from conventional MRIs.
The objective of this study was to highlight the role of DWI in differentiating benign from malignant complex adnexal masses.
Patients and methods
Twenty-five patients with adnexal masses underwent conventional MRI and DWI and the cases were proven by postsurgery pathological examination. Analysis of the pathological specimen with lesion morphology, signal characteristics, and correlation with the appearance at DWI followed by apparent diffusion coefficient values measurement were obtained.
Twenty-five patients with adnexal mass lesions were included. Included masses proved benign in 18 (72%) and malignant in seven (28%). Restricted diffusion was observed in proved malignant masses (24%, n = 6/25). Benign tumors with high DWI signal intensity evidence at 24% also. The mean apparent diffusion coefficient value was 1.4+0.34×10−3 and 1.02+0.06×10−3 mm2/s, for benign and malignant masses, respectively.
DWI supported by conventional MRI data can confirm or exclude malignancy in suspicious ovarian masses. A combined analysis of quantitative and qualitative criteria and a knowledge of the sequence pitfalls are required.

Keywords: apparent diffusion coefficient, adnexa, diffusion-weighted imaging, MRI

How to cite this article:
El-Sayed ESM, Abdullah MS, Ali HG. The role of diffusion-weighted MRI on the differentiation of complex adnexal masses. Menoufia Med J 2019;32:881-8

How to cite this URL:
El-Sayed ESM, Abdullah MS, Ali HG. The role of diffusion-weighted MRI on the differentiation of complex adnexal masses. Menoufia Med J [serial online] 2019 [cited 2020 May 31];32:881-8. Available from: http://www.mmj.eg.net/text.asp?2019/32/3/881/268799

  Introduction Top

Ovarian cancer is the seventh most common malignancy among women worldwide representing 3.7% of all cases of cancer in women and the second most common gynecological malignancy after cervical cancer [1]. It is a disease of postmenopausal women and sometimes prepubescent girls. Risk factors include age more than 50 years, positive family history, infertility, and previous cancer. Ovarian malignancy is usually discovered at the late stage (stages III and IV) with a 5-year survival rate of 20%. Fortunately, if the disease is discovered earlier (stage I), the 5-year survival rate will increase to 90%. Recurrence of ovarian cancer in spite of aggressive treatment is common [2],[3],[4].

Most malignant ovarian tumors are primary (95%) usually of epithelial origin (90%). The epithelial tumors are classified into serous, mucinous, endometrioid, clear cell, and undifferentiated. The nonepithelial tumors include sex cord stromal tumors and germ cell tumors (dysgerminoma, teratoma, yolk sac, and choriocarcinoma). Most primary tumors that metastasize to the ovary include gastric and colorectal (which are also called Krukenberg tumors), breast, pancreas, and melanoma [5].

Excessive surgical procedures such as bilateral oophorectomy with or without hysterectomy have sometimes been performed in patients with benign ovarian tumor because the preoperative diagnosis was inaccurate [6].

Preoperative diagnosis of ovarian tumors based on imaging is important as biopsy is not commonly applicable [7]. Ultrasonography (US) is the first-line imaging modality for adnexal lesions and is a particularly useful preoperative test for the characterization of noncomplex masses. MRI may be of great help in identifying malignant lesions before surgery, particularly when US findings are suboptimal or indeterminate [8].

MRI displays morphological characteristics and signal intensity variations on T1 and T2 weighted images (WIs) for the diagnosis of ovarian masses. Features such as papillary projections, mural nodules, thick septa, and solid components can be easily distinguished on MRIs; yet these criteria cannot reliably distinguish malignant from benign tumors.

With its multiplanar capability, superior tissue contrast and different sequences, MRI becomes a crucial method of investigation of ovarian lesions. MRI has high sensitivity (97%) and specificity (84%) in characterizing malignant lesions and solves the problem of indeterminate lesion on US [1].

Conventional MR sequences include T1, T2, and fat-suppressed images which provides anatomical and morphological criteria of the lesion. Lesions with high signal on T1 (fat or blood) and low signal in T2 (fibrous tissue) are likely to be benign [9]. In contrast, solid lesions with necrosis, cyst with irregular wall or septum or presence of solid and cystic components within the lesion are more likely to be malignant [10]. Administration of contrast agent, for example, gadolinium-DTPA with the use of fat suppression can differentiate between the enhanced solid component and nonenhanced debris and blood clots [1].

Diffusion-weighted imaging (DWI) is an in-vivo functional method of investigation of various pathological conditions [11]. Diffusion-weighted MRI (DW-MRI) is a technique that provides a noninvasive evaluation of the extent of microscopic diffusion present within biological tissues. For example, DW-MRI can characterize tissues with respect to cell organization and density, microstructure, and microcirculation on the basis of the water diffusion properties associated with each of these aspects.

It can be obtained by ultrafast spin-echo echoplanar T2-WI with parallel imaging. As a modification of T2 sequence, DWI requires application of two diffusion-sensitive gradients to the classic spin-echo sequence (paired gradients). One of them is the dephasing gradient applied just before the 180° rephrasing pulse and the other gradient applied after the 180° rephrasing pulse. Both gradients should cancel each other and the tissue with restricted diffusion will be fully rephrased and hence preserve its T2 signal while the tissue with free diffusion, the water molecules move significantly between the two gradients and would not be fully rephrased which results in loss of its T2 signal intensity [12],[13],[14].

Apparent diffusion coefficient (ADC) is a quantitative derivative of DWI that can be expressed as a map or calculated as a value. Multiple b-values should be obtained to reduce the error in ADC calculation and improve tissue characterization [15].

  Patients and Methods Top

This study is a prospective analysis that was conducted in a government hospital from October 2016 to September 2017. The study was approved by the Ethical Committee of Menoufia Faculty of Medicine and an informed consent obtained from all participants. After full explanation of the benefits and risks of the procedure.

Twenty-five patients with adnexal masses were included that fulfilled the following inclusion criteria: complex solid/cystic patterns, vegetation and/or septations in cystic masses, and large mass size.

We excluded masses with purely simple cystic lesions and cases of general contraindications of MRI scan such as cardiac pacemakers, ferromagnetic aneurysm clips, cochlear implants, and metallic foreign bodies.

The age of the patients ranged from 22 to 67 years (mean age: 41.68 years). Their symptomatology included abdominal enlargement, nonspecific pelvic pain, dysuria, frequency of micturition, and weight loss. The patients were referred based on preliminary ultrasound examination.

All cases had undergone preliminary transabdominal/transvaginal pelvic US on an ultrasound machine GE (General Electric Company, Boston, USA) logic using a 3–4 MHz abdominal convex probe and 7–8 MHz for the transvaginal one.

All studies were performed using a 1.5-T MRI unit (Entra and Achieva; Philips Medical System, Eindhoven, The Netherlands).

The patients were instructed to fast for 3 h and void urine 2 h before examination. Intravenous administration of 10 mg of an antispasmodic drug (hyoscine butylbromide) was given immediately before MRI to reduce bowel peristalsis.

All patients were imaged in supine position using a pelvic phased-array coil. Conventional routine pelvic MRI was performed followed by DWI sequence, using the following protocol: Conventional T2 axial, sagittal, and coronal were obtained with TR range/TE range: 3000–5000/90–100 and field of view (FOV): 288×350, 290×290, and 300×300 mm, respectively, T2 axial SPAIR, T1 axial with TR/TE: 500/10, and FOV: 260×216 mm. Fat-suppressed T1 axial and coronal postcontrast images were obtained after injection of intravenous contrast (Magnevist) 0.1 ml/kg with TR range/TE range: 420–500/10 and FOV 260×216 and 280×280 mm, respectively. DW axial images were obtained with b-values of 0, 500, and 1000 mm 2/s, TR/TE was 5000/77, FOV of 240×240 mm, matrix size of 124×100, and slice thickness was 6 mm with a 1 mm slice gap. Contrast media were not used in four cases because of renal dysfunction in one case and contrast sensitivity in the other three cases.

Conventional MRI and DWI findings were interpreted by two experienced radiologists.

First, the conventional MRIs were analyzed to detect the location (unilateral or bilateral), morphology regarding the size; components either cystic, unilocular or multilocular, complex solid, and cystic or predominately solid; signal intensity in T1, T2, and postenhancement criteria of the lesion (homogeneous, heterogeneous, or marginal).

In our MRI interpretation, following Valentini et al. [16] we considered criteria for the prediction of ovarian malignancy: mass size more than 4 cm, cystic masses with thickness more than 3 mm of the walls and septa, internal structure (papillary projections, nodularity, various degrees of solid components, necrosis, and hemorrhage) associated ascites, peritoneal deposits, and lymphadenopathy. Criteria suggesting benignity of the lesion: entirely simple cyst, size less than 4 cm, no solid components, thickness of the wall and septae less than 3 mm, and no ascites nor lymphadenopathy.

Following Mohaghegh and Rockall [1], we considered the signal characteristics for benign pelvic masses: high signal intensity on T1-WI is considered either fat or blood (e.g. dermoid/teratoma and endometrioma). On fat-suppressed images low signal is noted with fat, whereas high signal is still noted in the blood. Solid masses with very low signal intensity in T2-WI are characteristic to fibrous tumor (e.g. ovarian fibroma, Brenner tumor, or pedunculated subserous fibroid).

Masses of interest scanned using the b-values: 0, 500, and 1000 mm 2/s. DWIs with a b-value of 0 and 500 s/mm 2 were not evaluated because of the displayed less diffusion and larger T2 shine-through effect which were noted in eight cases, yet they are needed to provide a postprocessing ADC map with a good resolution and consequently develop an accurate measurement of the ADC value.

DWIs were inspected for the presence of persistent high signal intensity (restricted diffusion) and low ADC in correlation with the solid components of the included masses. Lesions with high signal on T2, DWI, and ADC map were attributed to T2 shine-through effect and not to true diffusion restriction. Lesions with low signal in DWI and high signal in ADC were considered facilitated diffusion. Lesions with low signal in both DWI and ADC were considered T2 blackout effect of dense fibrous tissue.

We measured the ADC values by manually applying region of interest (ROI) on the solid portions of the masses. ROI was specifically placed at areas of bright signal intensity on DWIs. For masses with an obvious solid component, a large ROI was applied to cover as much as possible of the pathology, in case of masses with vegetation or thickened septae; multiple ROIs were applied to the areas of concern and their mean was calculated.

The conventional MRI and DWI suggested pathology were compared whether benign or malignant in correlation with surgical pathology specimens which is the gold standard of reference.

Computer software package SPSS 15.0 (IBM in Armonk, New York, United states) was used in the analysis. For quantitative variables, mean (as a measure of central tendency) and SD (as measures of variability) were presented. Frequency and percentages were presented for qualitative variables, sensitivity, and specificity; positive predictive value (PPV), negative predictive value (NPV), and accuracy were all calculated for the conventional MRI and for the DWI. t-Test was used to estimate the differences in quantitative variables. A P value of less than 0.05 is considered to be significant.

  Results Top

This study included 25 patients that showed up with 25 complex cystic or solid adnexal masses selected after a preliminary pelvic ultrasound examination. The patients with benign tumors showed an age range of 25–65 years (mean age: 41.6 ± 13.8 years), whereas the age of those with malignant tumors ranged from 22 to 67 years (mean age: 46.2 ± 10.676 years).

Masses included 18 (72%) benign and seven (28%) malignant pathologies. Benign tumors included three mature teratoma, two serous cystadenoma, four pedunculated subserous fibroids, three mucinous cystadenoma, two tubo-ovarian abscess, two pyosalpinx, one ovarian fibroma, and one broad-ligament fibroid. Malignant tumors included: two mucinous cystadenocarcinoma, one clear-cell carcinoma, one granulosa cell tumor, two peritoneal papillary cell carcinoma, and one immature teratoma.

The minimum and maximum dimensions of benign masses were 3 and 13 cm, respectively, with a mean of 11.5±4.45 cm. Malignant tumors showed minimum and maximum dimensions of 7 and 20 cm, respectively, with a mean of 13.5±5.2 cm.

One case only that was presented by bilateral adnexal masses and rest of the cases presented as unilateral masses.

Masses were presented by various morphological features, multilocular (n = 9), unilocular (n = 0), complex cystic and solid (n = 7), and solid [9].

The complex adnexal masses showed variable signal intensities in T1 and T2 of the soft tissue components as follows: signal intensities of the masses in T1: masses elicited intermediate signal intensity in T1 (60%), bright signal (12%), and low signal (28%). Signal intensities of the masses in T2: masses elicited intermediate signal intensity in T2 in about 44%, bright signal intensity in 40%, and low in 16%.

Masses showed different patterns of postcontrast enhancement as follows: homogeneous (n = 6), heterogeneous (n = 8), wall/septae enhancement (n = 5), and marginal (n = 2).

Regarding the malignant masses: All of the malignant masses showed a wall thickness of more than 3 mm (100%), vegetation of more than 1 cm (100%), one mass was associated with moderate ascites (14%), but none of them showed concomitant pathologically enlarged lymph nodes or enhancing peritoneal nodules.

Diagnosis of complex adnexal masses

We compared the number of cases which was diagnosed by the conventional MRIs as benign or malignant tumors according to the criteria mentioned before, with those diagnosed depending on the DWI. The results were compared with the pathology which is considered the main reference. The conventional MRI suggested benignity in 17 cases and malignancy in eight cases. However, DWI suggested benignity in 13 cases and malignancy in 12 cases. But the pathology confirmed benignity in 18 cases and malignancy in seven cases.

[Table 1] shows signal intensities of the pathological entities presented in the study regarding DWI at different b-values and corresponding ADC map.
Table 1: Signal intensities of the pathological entities presented in this study regarding diffusion-weighted imaging at different b-values and corresponding apparent diffusion coefficient map

Click here to view

Conventional MRI suggested malignant pathology in eight tumors as being malignant, seven of them were true malignant, and one was proved to be benign.

DW-MRI showed restriction in six truly malignant masses as in [Figure 1] and other six cases showed restriction in spite of their benignity (false positive) proved by the pathology. These include the following entities: mature cystic teratoma [Figure 2] (n = 2), tubo-ovarian abscess (n = 2), pyosalpinx (n = 2), and showed facilitated diffusion in one case which is diagnosed as malignant by pathology (false negative). This could be attributed to the well differentiated and low-cellularity nature of the lesion [Table 2].
Figure 1: A premenopausal 42-year-old woman who gave an informed written consent with bilateral ovarian masses: (a and b) axial T2-weighted and axial T1-weighted (left image) fast-spin echo showed bilateral ovarian complex masses with soft tissue components showing postcontrast enhancement; (c and d) axial diffusion-weighted imaging with a b-value of 1000 showed high signal intensity at the solid components with corresponding low signal intensity at apparent diffusion coefficient map; (e) the pathology proved malignancy with bilateral ovarian mucinous cystadenocarcinoma.

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Figure 2: A 25-year-old woman who gave an informed written consent with right-side ovarian mature teratomas: (a) axial T2-weighted, (b) axial T1-weighted image, (c) axial T1-weighted image fat-sat, (d) axial T1-weighted image postcontrast, showing a right-side adnexal complex lesion with a fatty component that elicits bright signal in both T1 and T2 that is suppressed in the fat-sat sequence. It shows restricted diffusion with bright signal at a b-value of 1000 (e), and intermediate apparent diffusion coefficient map signal measuring about 0.8 mm2/s (f).

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The different ADC values elicited from the corresponding ADC maps were calculated [Table 2].
Table 2: The different apparent diffusion coefficient values of the included masses

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The sensitivity, specificity, PPV, NPV, and accuracy were calculated for conventional MRIs and DWI. The conventional MRI had 85.7% sensitivity, 88.8% specificity, 75% PPV, 94.1% NPV, and 88% accuracy. DWI had 85.7% sensitivity, 66.7% specificity, 50% PPV, 92.3% NPV, and 72% accuracy.

  Discussion Top

The primary goal of imaging in the evaluation of an adnexal mass is to differentiate malignant from benign. Proper diagnoses will direct patients to the appropriate treatment algorithm to reduce the number of women unnecessarily undergoing cancer surgery, to preserve fertility in young women (by allowing laparoscopy), and, when necessary, to enable the referral of patients to a tertiary referral center with a specialist gynecologic oncologist [17].

Currently, there is no gold standard for the diagnosis of a benign adnexal tumor versus a malignant ovarian tumor before surgery, especially when the tumor has both solid and cystic components. The MR data that is used for the prediction of ovarian malignancies include lesion size (>6 cm), thickness of the walls and septa (>3 mm), and the detection of internal structures including papillary projections, nodularity, various degrees of solid components, necrosis, hemorrhage, or regions of striking enhancement following administration of contrast medium [18].

However, these imaging parameters have been found to overlap for benign and malignant ovarian lesions.

Therefore, as proposed by Thomassin-Naggara et al. [18] the above-mentioned parameters are not always the most accurate predictors of ovarian malignancies. For example, in a recent series of 168 ovarian masses, papillary projections (vegetation) or nodularities were present in 37.5% of benign ovarian epithelial tumors. Further histological analysis demonstrated that these vegetation were present in 20–26% of the benign tumor samples assayed in 62–78% of the borderline tumors assayed, and in 59–92% of ovarian cancers assayed. Similarly, MRI detected vegetation were present in 13–22, 61–62, and 38–48% of benign, borderline, and invasive ovarian cancers, respectively [19].

Correspondingly, a diagnosis based on vegetation characteristics alone was associated with poor sensitivity and specificity.

DWI is one of the functional imaging techniques that have shown to be effective in the differentiation of benign from malignant adnexal masses. DWI provides functional information about the microenvironment of water in tissues, hence augmenting the morphologic information derived from conventional MRIs. It can depict shifts of water from extracellular to intracellular compartments, altered cell membrane permeability, disruption of cell membrane depolarization, and increased cellular density. Such changes may be associated with tumors [20].

In 2004, there was an initial experience that tried to determine the feasibility of using ADC measurement for the differential diagnosis of malignancy in only 12 cases. The research was descriptive rather than analytic and the main challenge at that time was image motion artifact. Finally the study group concluded that ADC measurement, intensity, and texture have the capability to distinguish malignancy in ovarian masses [21]. Since then, several studies have analyzed the added value of DWI to conventional MRI protocol to differentiate benign from malignant adnexal/ovarian tumors.

In this study, we had performed an individual analysis for the conventional MR sequences and DWI regarding their diagnostic performance in the evaluation of complex adnexal masses.

Masses differentiation on the conventional MR was based on the morphological features which is a very important issue that was considered for many years.

Blinded evaluation was done for the functional data supplied by DWI regardless of specific signal intensity of the masses included in the conventional series.

The aim of such performance was to get an unbiased judgment for the utilized MRI tools of assessment and to find out whether DWI is a necessity or luxury in case we need to assess an adnexal mass.

According to this study, DWI had shown 85.7% sensitivity in its individual performance during the assessment of the included adnexal masses, yet the specificity was low (66.7%). Such low specificity elicited in our research is explained by the presence of six benign masses that have mimicked malignancy on DWI, starting from their misleading signal intensities of restricted diffusion, down to the low ADC values measured. Such masses included: mature cystic teratomas (n = 2), tubo-ovarian abscess (n = 2) and pyosalpinx (n = 2) showed restricted diffusion and mean ADC values of 0.6×10-3 mm 2/s (false positive), due to mixed cellularity of the teratoma.

In our study, although some overlaps were found in the ADC values of benign and malignant lesions, the mean ADC value of malignant ovarian masses was significantly lower than that of benign. The mean ADC values for malignant lesions were 1.02±0.38×10-3 mm 2/s, whereas that for benign lesions were 1.4±0.5×10-3 mm 2/s.

Focusing on the quantitative and not the qualitative analysis of DWI was the purpose of a Turkish study which evaluated 59 ovarian masses. The study group declared that the ADC values of benign and malignant ovarian lesions overlap and DWI cannot be used for discrimination [22]. The drawback in their analysis is the unawareness about DWI pitfalls. They included purely cystic lesions such as endometriomas, hemorrhagic cysts, and dermoid cysts, which in spite of being cystic present with low ADC values and so can overlap with those of malignant masses. Also the studied sample size was limited.

Another study was carried out by Fujii et al. [23] on 123 ovarian masses that included 42 malignant and 81 benign lesions. In this study, the majority of the malignant tumors, mature cystic teratomas, and almost half of the endometriomas showed abnormal signal intensity on DWI, whereas most fibromas and other benign lesions did not. The main locations of abnormal signal intensity were solid portions in malignant ovarian tumors, keratinoid substances, and Rokitansky protuberance in mature cystic teratomas, and intracystic clots in endometriomas. They finally concluded that DWI of ovarian lesions and the elicited ADC values are not useful for differentiating benign from malignant ovarian lesions. Another study was carried out by Zhang et al. [8] on 191 patients with 202 ovarian masses; the purpose of this study was to evaluate the differences in ADC values for the solid component of benign and malignant ovarian surface epithelial tumors with the goal of differentiating benign versus malignant ovarian tumors preoperatively.

The results of that study showed that DWI appears to be a useful method for differentiating between benign epithelial ovarian tumors with solid components and malignant ovarian tumors, and is associated with high sensitivity and specificity, however, after exclusion of endometriomas, mature cystic teratomas and pure cystic adenomas from the analysis.

Considering such exclusion may have elevated the specificity of the DWI in our study, yet this was not applicable; first, because our analysis is a prospective evaluation and second such action would have subjected our evaluation to a major bias and unreliable data for use in clinical practice.

Thomassin-Naggara et al. [18] evaluated the contribution of DWI in conjunction with morphological criteria to characterize 77 complex adnexal masses (30 benign and 47 malignant). In their results, low signal intensity both on DWI and T2-WIs in the solid component of mixed adnexal masses would predict benignity and could help in differentiating benign from malignant lesions. This result matches with our study as we have six cases (four pedunculated subserous fibroid, one broad-ligament fibroid, and one ovarian fibroma), presented with low signal on T2-WI and DWI with respect to malignant masses. These results matched with our result.

The strength of this study lies in the use of the advantages of DWI as well as took care of the sequence pitfalls in assessment. Moreover, DWI can be used as an alternative to contrast sequences for patients with renal failure and in case of pregnancy. In this study, four patients have benefitted from such advantage. Conventional MRI combined with DWI was able to provide accurate diagnose in all of them. Despite these advantages, there were also limitations associated with this preliminary study. For example, the population of patients evaluated was not large. Therefore, our results will need to be confirmed in larger clinical studies. Second, this study only included cases of complex ovarian tumors, and not purely cystic tumors. As a result, the observations made might not be directly applicable to all of the cases evaluated in the clinic.

  Conclusion Top

The solo performance of DWI is not an applicable way to discriminate benign from malignant ovarian masses. DWI can confirm or exclude potential malignancy in suspicious ovarian masses, provided (i) inclusion of the conventional MRI data, (ii) combined analysis of DWI quantitative and qualitative criteria and (iii) awareness of the sequence pitfalls.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

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Conflicts of interest

There are no conflicts of interest.

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