Diffusion-weighted MR imaging for differentiating borderline from malignant epithelial tumours of the ovary: pathological correlation

Introduction

Borderline epithelial ovarian tumours (BEOTs), also known as tumours of low malignant potential, account for 4–14 % of all epithelial ovarian tumours (EOTs).

Although uncommon, peritoneal implants or metastatic lymphadenopathy may occur in patients with BEOTs. Clinically, BEOTs are distinct from ovarian malignant epithelial tumours (MEOTs) in that they often affect young women of childbearing age.

Patients with BEOTs are more likely to have early stage disease, and generally have an excellent prognosis after surgical excision but a high recurrence rate.

It is important to preoperatively discriminate BEOTs from MEOTs because a conservative fertility-sparing laparoscopic surgery can be performed in the former.

Magnetic resonance (MR) imaging is gaining recognition as a complementary method to ultrasound in the diagnosis of complex adnexal masses because of its excellent capacity for tissue characterization.

The addition of DW imaging to conventional MR imaging seems to improve accuracy in differentiating benign from malignant ovarian lesions.

Concerning ovarian lesions; Thomassin-Naggara reported that simultaneously low signal intensity within the solid component on T2-weighted and on b 1000 DWI suggested benignity of complex adnexal mass.

To authors’ knowledge, the utility of DW imaging in the differentiation of BEOTs and MEOTs has not been reported.

The purpose of this study was to investigate whether DWimaging is a useful tool in distinguishing BEOTs from MEOTs.

Materials and methods

Study population

This retrospective study was approved by authors’ institutional review boards and informed consent was obtained from all patients.

Patients with suspected ovarian tumours on the basis of elevated CA 125 level, ultrasound or CT were enrolled in an ovarian tumour MR imaging study project from October 2009 to September 2012.

Among 365 cases proven by surgery and pathology, a total of 102 patients were found with non-benign EOT including 60 BEOTs in 48 patients and 65 MEOTs in 54 patients.

Study population

Patients’ ages ranged from 17 to 71 years (mean, 39.5±15.3 years) in the borderline group and 40–75 years (mean, 55.3±9.4 years) in the malignant group.

The radical surgery, consisting of TAH+BSO, omentectomy, multiple peritoneal biopsies, retroperitoneal lymph node sampling, and cytological analyses of ascitic or peritoneal lavage fluid, was performed in 70 patients (16 patients with BOETs and 54 patients with MEOTs).

The non-conservative surgery of BSO with or without hysterectomy was performed in 19 patients with BEOTs.

The conservative surgery of unilateral salpingo-oophorectomy was performed in 13 patients with BEOTs.

MR imaging technique

MR imaging was performed using a 1.5-T unit (Avanto or Symphony, Siemens, Erlangen, Germany) with a phased array coil.

Spasmolytic drugs were not administrated.

Patients in the supine position breathed freely during acquisition.

The imaging range was from the inferior pubic symphysis to the renal hilum and was extended beyond the dome of tumour in the cases with huge masses.

MR imaging technique

Routine pelvic MR images were acquired as follows: Axial T1-weighted imaging (T1WI).

Axial T1WI with fat suppression

Axial and sagittal T2-weighted imaging (T2WI) with or without fat suppression.

Axial DW imaging was then obtained using echo planer imaging sequence with diffusion gradient b factors, 0 and 1,000 s/mm2; and acquisition time, 2 min 46 s.

Axial dynamic gadolinium-enhanced fat-suppressed T1WI was performed immediately after intravenous injection of 0.1 mmol/kg of contrast material at a flow of 2.5 ml/s;

MR image analysis

MR images were read by two radiologists in consensus with 10 and 29 years of experience in gynaecological imaging.

Both of the radiologists were blinded to the clinical data of patients.

The morphological features (tumour size, presence of solid component) were determined on T2WI and contrast-enhanced T1WI.

The term “solid component” included the solid portions, papillary projections and thickened septa (larger than 5 mm).

MR image analysis

The signal intensity (SI) of tumour on DW imaging was classified as high (similar to the SI of nerve root), moderate (similar to small intestine) or low (lower than small intestine).

On the ADC maps, a circular region of interest (ROI) of at least 1 cm2 was placed at targeted areas with the possibly lowest ADC values in the cystic and/or solid components of tumour, by referring to conventional MR images, including contrast-enhanced images and carefully avoiding areas such as haemorrhage, necrosis, major vascular structures, and artefacts such as chemical shift and magnetic susceptibility artefacts.

MR image analysis

To eliminate the potential influence of intraindividual correlation in patients with bilateral tumours (n=23), only the results for the most complex tumour were considered; thus, 102 tumours (48 BEOTs, 54MEOTs) were evaluated.

Also the analysis of ADC values of solid components smaller than 10 mm (10 BEOTs and 3 MEOTs) were excluded because of low contrast-to-noise ratio and motion artefacts.

At least three measurements were obtained and averaged.

Histopathological evaluation

The histopathological examination was performed by a pathologist with 12 years of experience in gynaecological pathology.

After that statistical analysis was performed.

Results

Pathological findingsGross pathology confirmed MR morphological findings.

DW imaging findings

The mean ADC value and DW imaging SI of the cystic component did not differ significantly between the two groups.

Axial T2- weighted with fat suppression (a) and T1-weighted contrast enhanced images (b) demonstrate a cystic mass with multiple septa and a papillary projection extending from the cyst wall. The projection (arrow) shows high signal intensity on DW imaging (c) and has an ADC value of 0.607×10−3 mm2/s (d)A 42-year-old woman with ovarian mixed adenocarcinoma.

Axial T2-weighted with fat suppression (a) and T1-weighted contrast enhanced images (b) demonstrate a solid mass (arrow). The mass shows high signal intensity on DW imaging (c) and has an ADC value of 0.891×10−3 mm2/s. A 40-year-old woman with ovarian serous adenocarcinoma.

Axial T2-weighted with fat suppression (a) and T1-weighted contrast-enhanced images (b) show a unilocular cystic lesion with a large papillary projection demonstrating obvious contrast enhancement (arrow). The papillary projection shows moderate signal intensity on DW imaging (c) and has an ADC value of 1.486×10−3 mm2/s (d).

A 20-year-old woman with ovarian serous borderline tumour.

Axial T2-weighted with fat suppression (a) and T1-weighted contrast enhanced images (b) demonstrate a right-sided solid mass (arrows) and a left-sided cystic mass with intracystic papillary projections. The solid component shows low to moderate signal intensity on DW imaging (c) and an ADC value of 1.975×10−3 mm2/s and 1.869×10−3 mm2/s in the right and left masses, respectively. A 27-year-old woman with bilateral ovarian serous borderline tumours.

Discussion

MR imaging has shown a high diagnostic specificity for some types of ovarian masses, such as dermoid cysts, endometrial cysts and fibromas. However, there is no specific role for conventional MR imaging in characterizing borderline and malignant EOTs.

The presence of a contrast-enhanced solid component may be useful for distinguishing malignant from benign epithelial tumours but not for borderline from malignant tumours.

In this study, most (54/60) BEOTs demonstrated at least one of the imaging features which were recognized to be associated with malignancy, such as irregularly thickened wall, enhancing vegetation and predominantly solid mass.

Some studies show that DW imaging can differentiate malignant from benign ovarian tumours with higher DWI SI and lower ADC values in malignant tumours. However, no significant ADC value difference was found between the two groups.

The inconsistent results are probably due to the diversity of samples and histopathological complexity of the ovarian tumours.

Also some benign solid tumours such as teratomas or fibrothecomas have lower ADC values that compromise the higher ADC values in benign and borderline epithelial tumours.

So, in this study, these non-epithelial tumours were ruled out because of their characteristic findings on conventional MR imaging.

In this study, most BEOTs demonstrated low or moderate SI in the solid component on DW imaging, whereas almost all MEOTs demonstrated high SI in the solid component.

The mean ADC value of the solid component in BEOTs was much higher than in MEOTs.

Furthermore, the study showed an optimal ADC value threshold of 1.039×10−3 mm2/s for differentiating borderline from malignant tumours with a sensitivity of 97.0%, a specificity of 92.2% and an accuracy of 96.4 %.

When the solid component was too small to measure the ADC value, a high DW imaging SI often suggested a MEOT.

Therefore, both the assessments of DW imaging SI and ADC value were useful in differentiating BEOTs from MEOTs.

Although the radical surgery is the usual treatment for BEOTs, the need for this procedure is controversial, as no significant differences in the recurrence and mortality between patients with radical and conservative surgeries have been observed.

The conservative surgery has been recommended in young patients with an early stage BEOT, even with a stage II, III or IV BEOT, if they wish to maintain their fertility.

The accurate characterization of BEOTs in the present study will encourage the implementation of conservative fertility-sparing surgery, especially the minimally invasive laparoscopic surgery.

Limitations of the study

First, DW imaging was acquired through free-breathing imaging which may affect the ADC value of lesions, especially huge cystic lesions.

Second, the precise matching of histological specimens taken for cell density measurement to the ADC value measurement of the tumour may be difficult in the mucinous BEOTs.

Third, the ADC value of solid component was not assessed in 10 of 48 BEOTs and 3 of 54 MEOTs, as the solid component was smaller than 1 cm.

Fourth, the ADC value threshold is machine-specific and probably not universal.

Conclusion

The utility of DW imaging can discriminate BEOTs from MEOTs, thereby improving the accuracy of pretreatment and surgical management of EOTs.

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