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ORIGINAL ARTICLE
Year : 2019  |  Volume : 67  |  Issue : 2  |  Page : 442-447

Prevalence and clinical characteristics of malformations of cortical development and incomplete hippocampal inversion with medically intractable seizures in Chennai – A prospective study


Institute of Neurology, Madras Medical College, Chennai, Tamil Nadu, India

Date of Web Publication13-May-2019

Correspondence Address:
Dr. R M Bhoopathy
Institute of Neurology, Madras Medical College, Chennai, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.258046

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 » Abstract 


Objective: To study the prevalence and clinical characteristics of malformation of cortical development (MCD) and incomplete hippocampal inversion (IHI) in adults with intractable seizures.
Materials and Methods: In this prospective study of 3220 epileptic patients in our epilepsy clinic between 2012 and 2014, 416 had intractable seizures. In all patients, a detailed clinical history, neurological examination, electroencephalography (EEG), computed tomography (CT) scan, magnetic resonance imaging (MRI) brain, and neuropsychological assessment was conducted to identify MCD and IHI.
Results: Out of 416 patients with intractable seizures, MCD and IHI were confirmed in 85 patients (48 males, 37 females). MCD was observed in 46 (11.05%) patients and IHI were observed in 39 (9.37%) patients. Chi square test revealed no signi cant difference between the MCD and IHI groups across the patients in different age groups, gender, type of seizure, duration and onset of seizure, seizure frequency, clustering, status epilepticus, EEG, febrile seizures, and family history. Statistically significant differences (P < 0.05) were observed between the MCD and IHI groups for change in seizure semiology and in intelligence quotient (IQ) and memory quotient (MQ) scores obtained using Wechsler's adult intelligence scale III and Wechsler's memory scale. The IHI group showed higher IQ and MQ scores when compared to the MCD group. Furthermore, IHI occurred along with MCD in 6.52% (N = 3) of the population.
Conclusion: MCD and IHI patients are often associated with intractable complex partial seizures. Intractable epilepsy patients with normal intelligence and normal MRI should be investigated with hippocampal volumetric studies to identify the presence of IHI. Isolated IHI can be considered as a form of MCD because it mimics the clinical features of MCDs.


Keywords: Focal cortical dysplasia, hippocampal volumetric study, incomplete hippocampal inversion, intractable epilepsy, malformation of cortical development
Key Message: Malformation of cortical development (MCD) and incomplete hippocampal inversion (IHI) can occur in equal proportion of patients with intractable epilepsy. Clinical characteristics of MCD and IHI were often similar, except the age of seizure onset, cognition, and change in seizure semiology. Patients with intractable seizures of the complex partial type with normal cognition without change in seizure semiology should be investigated for the presence of IHI. Histopathological studies may confirm IHI as a form of post-migrational gyral developmental malformation.


How to cite this article:
Bhoopathy R M, Arthy B, Vignesh S S, Srinivasan A V. Prevalence and clinical characteristics of malformations of cortical development and incomplete hippocampal inversion with medically intractable seizures in Chennai – A prospective study. Neurol India 2019;67:442-7

How to cite this URL:
Bhoopathy R M, Arthy B, Vignesh S S, Srinivasan A V. Prevalence and clinical characteristics of malformations of cortical development and incomplete hippocampal inversion with medically intractable seizures in Chennai – A prospective study. Neurol India [serial online] 2019 [cited 2019 Jul 16];67:442-7. Available from: http://www.neurologyindia.com/text.asp?2019/67/2/442/258046




Malformations of cortical development (MCD) are microscopic and macroscopic development abnormalities of the cerebral cortex that arise due to interruption in cortical development during fetal development by genetic or environmental factors.[1] According to Barkovich classification, MCDs are classified into three groups – (1) malformations due to abnormal neural proliferation, (2) malformations due to abnormal neuronal immigration, and (3) malformations due to abnormal cortical organization.[2] Due to improved magnetic resonance imaging (MRI) technology used among patients with epilepsy, a fourth group of MCD (not otherwise classified) has been added to the Barkovich classical classification.[3]

A meta-analysis of published and unpublished studies in India showed a prevalence rate of epilepsy in 5.35 per 1000 population.[4] The prevalence of intractable epilepsy in adults has been reported to vary from 15 to 20%.[5],[6],[7] There are very few studies in the literature reporting the prevalence of MCD in intractable epilepsy. The prevalence of MCD was reported to be high in intractable childhood epilepsy ranging from 25% to 40%.[7],[8] With recent advancements in radiological imaging techniques, the identification of MCD has increased significantly.

Most studies conducted on a group of patients with MCD reveal the most common types of MCD to be focal cortical dysplasia, polymicrogyria, lissencephaly, nodular heterotopias, dysembryonic neuroepithelial tumor, and hemimegalencephaly.[9],[10],[11] The clinical features of MCD are often heterogeneous. MCDs are generally reported to present with complex partial seizures more than any other form of seizures.[9] Thus, family history,[9] drug resistance and intractability,[10] change in semiology,[12] association with febrile seizures,[9] delayed motor or mental milestones,[9],[11] cognitive defects, and learning disability should be recorded.[11] Approximately one-third of patients with MCD have hippocampal abnormalities such as hypoplastic hippocampus, hippocampal sclerosis, malrotated hippocampus, and enlarged hippocampus.[11]

Incomplete hippocampal inversion (IHI) is a failure of hippocampal inversion that occurs during normal fetal development. It can be diagnosed with MRI and is often reported to be pathological in patients with seizures.[13] Recent studies among patients with temporal lobe epilepsy (TLE) and MCD have reported that IHI can be found in a similar proportion of patients with MCD and TLE.[14] An excellent study by Bajic et al., showed that IHI are observed in 30% of patients with epilepsy, mostly on the left side, followed by bilateral and right-sided IHI.[15] The presence of IHI has been reported to be a marker of a more extensive disorder of brain development.[14],[15] The evidence of having IHI as a malformation of brain development would possibly point towards its being the abnormality causing intractable epilepsy. There are no studies examining the clinical characteristics of the IHI population. As MCDs and IHI can occur in isolation as well as in combination, we carried out a prospective study to investigate the prevalence and clinical characteristics of MCD and IHI in intractable epilepsy. Thus, the study was conducted with the following aims: a. To estimate the prevalence of MCD and IHI in adults with medically intractable seizures; and, b. To prospectively explore the clinical characteristics of MCD and IHI in adults with intractable seizures.


 » Materials and Methods Top


A total of 3200 epileptic patients who were attending the epilepsy clinic at Rajiv Gandhi Government General Hospital, Chennai, were screened for intractable epilepsy between 2010 and 2014. Out of 3200 patients, 416 (239 male and 177 female) patients in the age range of 10–65 years had intractable seizures, constituting 13% of the total population.

A detailed clinical history and neurological examination were conducted on all the patients with intractable seizures. Their demographic data, educational and occupational history, seizure onset and duration, and seizure semiology were recorded. An interictal electroencephalography (EEG) was also performed for all patients with intractable epilepsy.

All patients underwent a conventional magnetic resonance imaging (MRI) with diffusion tensor imaging (DTI) on a 1.5-Tesla, 48-channel system (Seimens, Germany) using a head coil (40 element), gradient strength of 45 mT, and flow rate of 200 m/s. The MRI protocol consisted of axial T1-weighted sequence (T1), axial T2-weighted sequence (T2), and volumetric T1-weighted MRI (3D-SPGR; three-dimensional spoiled gradient echo) sequence. Volumetric analyses of the hippocampus were also carried out. These images were analyzed by experienced neuroradiologists who detected MCDs and hippocampal malformations. The criteria for IHI (malrotation of hippocampus) included incomplete rotation, abnormal rounded appearance of the head of hippocampus, blurry internal structure, changes in shape and size, and vertical orientation of the collateral sulcus. Patients fulfilling three of the several criteria were identified as having IHI.

The intelligence quotient (IQ) and memory quotient (MQ) were assessed by clinical neuropsychologists in patients presenting with MCDs and IHI using Wechsler's adult performance intelligence scale III and Wechsler's memory scale respectively. The Bender Gestalt test was also administered to assess the visual motor functions and simple visual recall.

Data collected from all patients with MCD and IHI were analyzed descriptively and statistically to estimate the prevalence, clinical characteristics, and association between both the groups (MCD as well as IHI).


 » Results Top


Prevalence of malformation of cortical development and incomplete hippocampal inversion

Out of 416 patients with intractable seizures, MCD and IHI were confirmed in 85 (48 male, 37 female) patients constituting 20.43% of the total population. MCD was observed in 46 (11.05%) patients and IHI was observed in 39 (9.37%) patients.

In 46 patients with MCD, various MCDs were observed, as described by the Barkovich classification.[5] Forty-six patients with MCD were grouped into group I, II, and III malformations, as seen in [Table 1].
Table 1: Various malformations observed in 46 patients with MCDs

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Focal cortical dysplasia was observed in various areas in the brain [frontal lobe (N = 9), temporal lobe (N = 9), occipital lobe (N = 1), insular lobe (N = 1), amygdala (N = 1), opercular region (N = 1), peritrigonal area (N = 1), and anterior claustrum (N = 1)].

Out of 39 patients with IHI, we observed IHI most commonly on the left-side in 87.17% (N = 34) patients when compared to the right-sided IHI that occurred in 12.82% (N = 5) patients. [Figure 1] shows the MRI images of patients with normal hippocampus and left-sided IHI.
Figure 1: 1.5T MRI image of a patient with intractable seizure with normal hippocampus (a) and left incomplete hippocampal inversion (b)

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Clinical features of malformation of cortical development and incomplete hippocampal inversion

Type of seizure

From [Figure 2], it can be inferred that the complex partial type of seizure is the most common type of seizure associated with both MCDs and IHI. 31 (67.4%) patients in the MCD group and 24 (61.5%) patients in the IHI group had complex partial seizures (CPS). Generalized tonic–clonic seizures (GTCS) were observed in 8 (17.4%) and 7 (17.9%) patients with MCD and IHI, respectively. Among MCD patients, 6 (13%) of them had simple partial seizures (SPS) and 1 (2.2%) patient had mixed partial seizure. Similarly in IHI patients, simple partial seizures (SPS) were present in 2 (5.1%) patients and mixed partial seizures in 2 (5.1%) patients. Myoclonic seizures and partial seizures with secondary generalization were observed in 4 patients (2 each) among the IHI group.
Figure 2: Type of seizures in 85 patients with MCDs and IHI. Note: GTCS (generalized clonic tonic seizure), SPS (simple partial seizure), CPS (complex partial seizure), PSSC (partial seizure with secondary generalization), MPS (mixed partial seizure),MS (myoclonic seizure), MPVOLH (left incomplete hippocampal inversion),FCD (focal cortical dysplasia), MPVORH (right hippocampal inversion), NH (nodular heterotopias), PMG (polymicrogyria), LIS (lissencephaly),DNET (dysembryonic neuroepithelial tumor), BH (band heterotopia), RtHM (right hemimegalencephaly), SC (schizencephaly), AGCC (agenesis of corpus callosum)

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Change in seizure semiology

When compared to the initial seizure history and the initial presentation of seizure, a change in the seizure semiology was observed in 38 (82.6%) patients in the MCD, and in 19 (48.7%) patients in the IHI group. In both the MCD and IHI groups, seizures initially presenting as generalized seizure later turned out to be of the complex partial seizure type. The chi-square test revealed statistically significant difference between the MCD and the IHI groups with respect to the change in seizure semiology (P = 0.002).

Age of onset

The age of onset did not vary significantly across the two groups (P = 0.461); 47.8% patients in the MCD group and 28.2% of patients in the IHI group had the onset of seizure at <5 years of age. Most patients with IHI had the age range of onset of seizure between 5 years to 20 years, as seen in [Figure 3].
Figure 3: Age of onset of seizures across the MCD and IHI groups

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Clustering and status epilepticus

A total of 28.26% (N = 13) patients in the MCD group and 46.15% (N = 18) patients in the IHI group did not show clustering of seizures. Seizures were reported to be observed in clusters of 1 in 10.9%, clusters of 2 in 39.1%, and clusters of 3 in 19.6% in the MCD group. In the IHI group, seizure clustering was observed in clusters of 2 in 30.8%, clusters of 3 in 15.4%, and clusters of 4 in 5.1% of the population. Status epilepticus was present in 8.7% (N = 4) in the MCD group and 7.7% (N = 3) in the IHI group. No significant differences were observed in clustering (P = 0.135) and status epilepticus (P = 1.00) between the MCD and IHI groups.

Cognitive functions

The IQ and MQ scores measured using Wechsler's adult intelligence scale III and Wechsler's memory scale showed statistically significant differences across the groups. The IQ and MQ in the MCD group were significantly lower than that in the IHI group (P < 0.05) when compared using chi-square test [Table 2]. In addition, the Bender Gestalt test showed significant brain dysfunction in the MCD group compared to the IHI group. Impaired visual motor function and simple visual recall were observed in 65.21% (n = 30) and 78.26% (n = 36) patients, respectively, of the MCD group. In IHI group, visual motor function and simple visual recall were impaired in 43.58% (n = 17) and 43.58% (n = 17) patients, respectively.
Table 2: Number of patients in the MCD and IHI group corresponding to their intelligence scores and memory quotient scores

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Electroencephalography studies

EEG was normal in 45.70% (N = 21) patients with MCD and in 52.6% (N = 20) patients with IHI. There was no relationship observed between the site of the lesion and the side of abnormal EEG recording. Moreover, there was no significant difference in the EEG findings between the MCD and IHI groups (P > 0.05).

Family history, febrile seizures, and neurocutaneous markers

Seven patients (15.2%) in the MCD group and 1 patient (2.6%) in the IHI group had a family history of seizures. 23.9% (N = 11) patients in the MCD group and 15.4% (N = 6) patients in the IHI group had febrile seizures. In the MCD group, neurocutaneous markers, such as adenoma sebacium, were observed in 2 patients and hypomelanosis of the skin was observed in a patient with hemimeganencephaly. In the IHI group, 2 had adenoma sebacium. No statistically significant difference (P > 0.05) was observed between the IHI and MCD groups related to these features.

Multiple pathologies

A total of 22.36% (N = 19) of the patients with MCD and IHI had dual or multiple pathologies in the brain. IHI was associated with MCD in 3 patients (6.52%), as seen in [Figure 4].
Figure 4: 1.5 T MRI T2 weighted images showing DNET in the right frontal region (a) and IHI in the left hippocampus (b)

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 » Discussion Top


In the present study, we prospectively analyzed 416 patients with intractable seizures to estimate the prevalence of MCD and IHI and its clinical characteristics. MCDs were observed in 46 (11.05%) patients with intractable epilepsy, which may be considered as ac omparatively low figure in our population compared to the other studies.[7],[8] This could be because the sample subjects considered for the present study were adults. In addition, the magnetic strength of MRI used in the present study would have caused reduced identification of MCDs and IHI.[16],[17] We also observed various types of MCD which were reported in the literature.[5],[9],[18],[19],[20],[21]

There are very few studies focusing on the prevalence of IHI in the epileptic population. The prevalence rate of IHI in the present study was 9.37% (39 patients), which is a figure similar to the prevalence rate of IHI (8.8%) in a group of 226 patients with febrile status epilepticus.[22] Similar to the various studies on IHI, the present study revealed that IHI is predominantly seen more on the left side when compared to the right side.[13],[15],[22] In contrary to the study by Chan et al.,[22] who observed bilateral IHI in the epileptic population but not on the right side, we found 5 patients with IHI on the right side and no cases with bilateral IHI. Even though MCD and IHI were less prevalent in our study population, they were observed in equal proportions in patients with intractable epilepsy.

Controversy exists in literature regarding the consideration of IHI as pathological in the epileptic population. Studies on IHI in healthy individuals have concluded IHI as a rare finding in patients without seizures.[13] A recent study by Cury et al.,[23] reported that IHI is a common left-sided phenomenon in normal individuals and is associated with morphological changes outside the medial temporal lobe. Though IHI may be observed in the normal population, it is stated to be pathological in patients with epilepsy.[14],[15] In our study, we found a significant number of patients with IHI having intractable epilepsy. Since the primary aim of the present study was to assess the prevalence and clinical characteristics of MCD and IHI among intractable epilepsy patients, we have not considered a control group to estimate the prevalence of IHI in normal individuals.

At present, only a few clinical features are known from the literature associated with IHI. Our study results correlate with the clinical features of IHI reported so far in the literature.[24],[25] IHI is often associated with partial epilepsy,[25] does not have direct memory repercussions,[24] and mostly exhibits left hippocampal changes.[15] Interestingly, in our study, we found that MCDs and IHI have similar clinical features except the age of seizure onset, the prevalence of cognition disorders, and the changes in seizure semiology, which can distinguish MCDs from IHI. The age of seizure onset is one of the predictors for intractable epilepsy along with structural abnormalities of the brain.[26] The age of seizure onset for the MCD group was less than 5 years; however, in the IHI group, it was between 5 and 20 years, which is supported by other studies.[9],[22],[26],[27],[28] MCDs varied from focal to multiple structural malformations in the brain resulting in normal to severe degree of cognitive impairments.[26],[27] Cognitive functions were fairly preserved in patients with IHI, which could be due to the noninvolvement of other brain structures. We also found that IHI can occur in isolation or in combination with MCD, occurring as forms of malformations secondary to the abnormal post-migrational gyral development.

From the present study, we infer that patients with intractable epilepsy with normal intelligence and normal MRI should be investigated with hippocampal volumetric studies to identify IHI. As IHI or hippocampal malrotation is a gyrational developmental defect, we propose that IHI be included as one of the varieties of MCD under group III.


 » Conclusion Top


The present study was carried out to estimate the prevalence and clinical characteristics of MCD and IHI in patients with intractable epilepsy. We found that MCD and IHI can occur in equal proportions of patients with intractable epilepsy, which could be identified using the conventional MRI and volumetric T1-weighted MRI (3D–SPGR) sequences. Clinical characteristics of MCD and IHI were often similar except for the age of seizure onset, cognition, and the change in seizure semiology. We conclude that IHI can be one of the causes for intractability of seizures in these patients. We emphasize that patients with intractable seizures of the complex partial type with normal cognition, having no change in the seizure semiology, should be investigated for the presence of IHI. Further histopathological studies may be performed in these patients to confirm IHI as a form of post-migrational gyral developmental malformation.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

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