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The value of double inversion recovery MRI sequence in assessment of epilepsy patients

The double inversion recovery (DIR) pulse sequence was introduced several years ago and since that it grew important value in clinical neuroimaging. We aimed to assess the added value of double inversion recovery in evaluation of epileptic patients. In mesial temporal sclerosis, the measured contrast parameters (SNR, CR, CNR and AI) were found to be significantly higher in DIR than in FLAIR and T2 sequences. In cases of focal cortical dysplasia, significantly higher CNR and AI in DIR than in T2 and FLAIR. Also DIR showed higher detection of the increased cortical thickness and cortical signal intensity than the T2 and FLAIR sequences. In tuberous sclerosis cases, the DIR showed higher visibility of the lesions than the T2 and FLAIR. Also DIR showed higher ability to detected grey-white matters junction blurring. Our study concluded that the greatest value of the double inversion recovery sequence is its higher ability in detecting multiple characteristics of the lesions in a one sequence.


Background
Epilepsy is a common chronic neurological brain condition that has wide range of causes with multiple influencing factors in most cases [1]. The MRI appears as a major player in its work up, however, a specifically tailored MRI protocol [2]. The Double inversion recovery (DIR) is appearing in the last few years to have a very important role in the neuroimaging as an excellent grey matter imaging modality [3].
Of the major causes of epilepsy appear the mesial temporal sclerosis and malformations of cortical development, as two of the most common causes of epilepsy among adult and pediatric age groups respectively [4,5]. Mesial temporal sclerosis (MTS) is characterized by neuronal loss and gliosis affecting selective parts of the hippocampal formation [6]. On the other hand, malformations of cortical development (MCDs) are a very wide and diverse range of disorders presented by multiple MR imaging features [7]. They include focal cortical dysplasias (FCDs), tuberous sclerosis (TSc), heterotopia, and polymicrogyria among other disorders [5,7,8].
MTS may represent a diagnostic challenge on MRI, as in the early stage, where the main findings of hippocampal sclerosis (the atrophy and T2 hyperintensity) are subtle [6,9].
Also, some of the malformations of the cortical development (MCDs) are difficult to characterize based on the current MRI modalities and they can mimic each other. So we conducted this study hoping that it can increase the efficacy of MRI in detecting the epileptogenic lesions so helping patients getting better management.

Methods
The study included 25 patients (18 females and 7 males). Their ages ranged between 1 and 57 years.

Inclusion criteria
25 consecutive patients with history of primary idiopathic epilepsy and their MRI revealed epileptogenic lesions were prospectively included in the study. All age groups were included.

Exclusion criteria
Patients with space occupying lesions, inflammatory pathology and vascular malformations.
All patients were subjected to B. Quantitative assessment: calculating average signal intensities of the lesions manually on the coronal DIR, FLAIR, and T2 images. For sake of comparison, the contralateral side for each lesion is further segmented and average intensity is measured. Then the signal-to-noise ratio (SNR), contrast to-noise ratio (CNR), contrast ratio (CR), and asymmetry index (AI) are calculated.
3. Lesions for visual analysis only: C. Other lesions: The examiners are asked to evaluate each lesion according to its visibility, where each lesion is classified as better, similar, or lower visible between DIR versus T2 and FLAIR sequences.

Statistical analysis
The statistical analysis of lesions on the different pulse sequences will be performed patient and lesion wise. All data will be gathered, statistically analyzed, and tabulated. Qualitative data will be described using number and percent. Quantitative data will be described using mean and standard deviation. Significance of the obtained results will be judged at the 5% level (P value of < 0.05 was considered statistically significant). Significance between periods was done using Post Hoc Test (adjusted Bonferroni) comparing between different periods using F test (ANOVA).

Assessment of patients with mesial temporal sclero-
sis: In the current study we assessed ten (10) patients with mesial temporal sclerosis with their mean age about 22.9 years (ages ranging between 17 and 35 years).
A. Visual evaluation: On T2, only six cases (60%) showed hyperintense signal in the affected hippocampus, compared to the contralateral side, the cortex and basal ganglia. While on FLAIR and DIR the hyperintense signal is detected within the affected hippocampus in all the ten cases (100%) compared to the contralateral side, the cortex and basal ganglia (Fig. 1) B. Quantitative assessment: the measured signal intensity was found to be higher in the ipsilateral side compared to the contralateral side in all the three sequences in 100% of cases.
Also, all the four contrast parameters (as shown in Table 2) were found to be significantly higher in DIR than in FLAIR and T2 sequences (P value of < 0.05 was considered statistically significant).

Assessment of patients with focal cortical dysplasia:
In the current study we assessed six patients with focal cortical dysplasia with their mean age about 11 years (ages ranging between 1 and 21 years on DIR than on T1, similar to that on T2 and better than on FLAIR (Fig. 3). Also, we found a single patient with grey matter heterotopia. The abnormality was almost equally visualized on DIR, T1 and FLAIR, and better visualized on DIR than on T2 (Fig. 4).

Assessment of patients with tuberous sclerosis:
In our study we found only two patients with tuberous sclerosis.    junction blurring out of the 19 lesions seen in the two patients (about 79%) (Fig. 5). 5. Assessment of patients with gliosis.
In our study, there were five patients showing gliosis. The results of their visual assessment were demonstrated in Table 5.  (arrow in a). Also, T2 and FLAIR show increased cortical thickness and hyperintense signal (arrows in b, c). The high signal intensity and increased cortical thickness are most conspicuous on the DIR image (arrow in d)

Discussion
In the visual assessment of mesial temporal sclerosis (MTS), there was a characteristic high signal intensity of the affected hippocampus in patients with MTS on DIR images, which was confirmed by the quantitative evaluation (in the form of SNR, CR, CNR and AI shown in Table 2. Our study agreed with what Qiong et al. [6] stated in their study, that DIR images can describe hippocampal sclerosis (HS) with high signal noise to ratio (SNR) and contrast to noise ratio (CNR), superior to conventional MR sequences (T2 and FLAIR sequences). However, our study showed significant increase in the contrast ratio (CR) and asymmetry index (AI) as well.
In case of focal cortical dysplasia, our study showed that the 3D DIR was capable to increase the detectability of some of the focal cortical dysplasia features, increased cortical thickness and cortical signal intensity in particular. Ryan [10] stated that the sensitivity and specificity of the DIR sequence for FCD among their observers ranged from 50 to 88% and 67-91% respectively and reached to conclusion that the DIR sequence is sensitive for the detection of focal cortical dysplasia, particularly when reviewed by experienced interpreters. Other researchers as Granata et al. [11] concluded that the main advantage of DIR acquisition could be its capability to demonstrate at the same time all the semiological characteristics of cortical development disorders.  In assessment of tuberous sclerosis patients, one of the cortical tubers was missed on T2 and FLAIR and only initially visualized on DIR. Also most of the lesions were better visualized on DIR than on FLAIR sequence. This can reflect the higher capability of the DIR sequence in lesion detectability over the T2 and FLAIR sequences. In the study by Cotton et al. [12] they found that in all their patients, the cortical tubers appeared very bright on the DIR sequence and were well outlined compared with high resolution T2 or FLAIR images and they concluded that DIR images may have a complementary role in the MRI evaluation of the tuberous sclerosis patients.

Conclusion
Our study concluded that the greatest value of the DIR sequence is its higher ability in detecting multiple characteristics of the lesions in a one sequence. Also, it should be clear that every MRI sequence has its value and the DIR is not to replace any of them, but to add to them in the sake of patient's benefit.

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