Prevalence, distribution, and clinical associations of suspected postictal changes on brain magnetic resonance imaging in epileptic dogs

Christian Maeso Anicura Ars Veterinaria, Barcelona, Spain

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Daniel Sánchez-Masian Anderson Moores Veterinary Specialists, Hursley, Winchester, UK

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Sergio Ródenas Animal Bluecare Veterinary Hospital, Málaga, Spain

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Cristina Font Canis Veterinary Hospital, Girona, Spain

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Carles Morales Anicura Ars Veterinaria, Barcelona, Spain

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Elisabet Domínguez Anicura Ars Veterinaria, Barcelona, Spain

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Jordi Puig Anicura Ars Veterinaria, Barcelona, Spain

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Juan Arévalo-Serrano Príncipe de Asturias University Hospital, Alcalá de Henares, Spain

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Patrícia Montoliu Anicura Ars Veterinaria, Barcelona, Spain

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Abstract

OBJECTIVE

To determine the prevalence of presumed postictal changes (PC) on brain MRI in epileptic dogs, describe their distribution, and recognize possible correlations with different epilepsy features.

ANIMALS

540 client-owned dogs with epilepsy and a complete medical record that underwent brain MRI at 4 veterinary referral hospitals between 2016 and 2019.

PROCEDURES

Data were collected regarding signalment, seizure type, seizure severity, time between last seizure and MRI, and etiological classification of epilepsy. Postictal changes were considered when solitary or multiple intraparenchymal hyperintense lesions were observed on T2-weighted and fluid-attenuated inversion recovery images and were hypointense or isointense on T1-weighted sequences, which were not confined to a vascular territory and showed no to mild mass effect and no to mild contrast enhancement.

RESULTS

Sixty-seven dogs (12.4%) showed MRI features consistent with PC. The most common brain sites affected were the piriform lobe, hippocampus, temporal neocortex, and cingulate gyrus. Dogs having suffered cluster seizures or status epilepticus were associated with a higher probability of occurrence of PC, compared to dogs with self-limiting seizures (OR 2.39; 95% confidence interval, 1.33 to 4.30). Suspected PC were detected both in dogs with idiopathic epilepsy and in those with structural epilepsy. Dogs with unknown-origin epilepsy were more likely to have presumed PC than were dogs with structural (OR 0.15; 95% confidence interval, 0.06 to 0.33) or idiopathic epilepsy (OR 0.42; 95% confidence interval, 0.20 to 0.87). Time between last seizure and MRI was significantly shorter in dogs with PC.

CLINICAL RELEVANCE

MRI lesions consistent with PC were common in epileptic dogs, and the brain distribution of these lesions varied. Occurrence of cluster seizures or status epilepticus, diagnosis of unknown origin epilepsy, and lower time from last seizure to MRI are predictors of suspected PC.

Abstract

OBJECTIVE

To determine the prevalence of presumed postictal changes (PC) on brain MRI in epileptic dogs, describe their distribution, and recognize possible correlations with different epilepsy features.

ANIMALS

540 client-owned dogs with epilepsy and a complete medical record that underwent brain MRI at 4 veterinary referral hospitals between 2016 and 2019.

PROCEDURES

Data were collected regarding signalment, seizure type, seizure severity, time between last seizure and MRI, and etiological classification of epilepsy. Postictal changes were considered when solitary or multiple intraparenchymal hyperintense lesions were observed on T2-weighted and fluid-attenuated inversion recovery images and were hypointense or isointense on T1-weighted sequences, which were not confined to a vascular territory and showed no to mild mass effect and no to mild contrast enhancement.

RESULTS

Sixty-seven dogs (12.4%) showed MRI features consistent with PC. The most common brain sites affected were the piriform lobe, hippocampus, temporal neocortex, and cingulate gyrus. Dogs having suffered cluster seizures or status epilepticus were associated with a higher probability of occurrence of PC, compared to dogs with self-limiting seizures (OR 2.39; 95% confidence interval, 1.33 to 4.30). Suspected PC were detected both in dogs with idiopathic epilepsy and in those with structural epilepsy. Dogs with unknown-origin epilepsy were more likely to have presumed PC than were dogs with structural (OR 0.15; 95% confidence interval, 0.06 to 0.33) or idiopathic epilepsy (OR 0.42; 95% confidence interval, 0.20 to 0.87). Time between last seizure and MRI was significantly shorter in dogs with PC.

CLINICAL RELEVANCE

MRI lesions consistent with PC were common in epileptic dogs, and the brain distribution of these lesions varied. Occurrence of cluster seizures or status epilepticus, diagnosis of unknown origin epilepsy, and lower time from last seizure to MRI are predictors of suspected PC.

Introduction

Epilepsy is one of the most common neurological disorders in dogs.1,2,3 MRI is considered the most valuable diagnostic tool for the investigation of structural causes of epilepsy.4,5,6 In human medicine, reversible MRI abnormalities in the postictal period, defined as postictal changes (PC), also termed peri-ictal changes, have been widely recognized and reported for many years.7,8,9 These lesions spontaneously resolve. They are classically visualized on MRI as areas of increased T2-weighted (T2W) signal intensity at different localizations, with variable alterations on diffusion-weighted imaging (DWI) and apparent diffusion coefficient. Moreover, they may show structural changes as mass effect secondary to brain swelling.10,11,12 Although the exact pathophysiology remains poorly understood,7 PC are thought to represent a combination of cytotoxic and vasogenic edema associated with increased energy metabolism, hyperperfusion, and cell swelling as a consequence of the ictal activity.8,9,10,13,14,15,16,17

Reported frequency of postictal MRI changes in human medicine is 15.9% in the general population with first epileptic seizures (ESs),17 whereas the prevalence in patients that suffered status epilepticus (SE) is highly variable, with published values from 11.6% to 63.3%.9,10,11,18,19 The described range of possible PC abnormalities is also wide, in terms of morphology, location, extent, gadolinium enhancement, and time course.9,10

In veterinary medicine, to the author’s experience, brain lesions resembling human PC changes are frequently identified in epileptic dogs. However, detailed description of these suspected PC changes is limited. In 2 previous reports including a total of 5 cases,20,21 lesions were located in the piriform, temporal, parietal lobes, or a combination of any of these locations and were hyperintense on T2W sequences, were hypointense on T1-weighted (T1W) images, produced mild to no mass effect, and showed variable postcontrast enhancement.20,21 Four cases were diagnosed with idiopathic epilepsy, and 1 case was diagnosed with structural epilepsy. More recently, 122 study and 123 abstract report additional brain locations for suspected PC in dogs with idiopathic epilepsy, including hippocampus, cingulate gyrus, caudate nucleus, thalamus, frontal, olfactory and occipital lobes. The majority of these dogs suffered from cluster seizures (CSs) or SE, and MRI was performed shortly after the last seizure episode. In a recent report, 79% of dogs were reported to suffer seizure activity 48 hours prior to MRI scan. The longest duration between last seizure episode and MRI-scan acquisition was 7 days. However, maximum time lapse between seizure and MRI detection of PC is currently unknown.22 To the best of the authors’ knowledge, there is a lack of information in the veterinary literature about the prevalence of presumed PC in the general epileptic dog population. Moreover, correlations between suspected PC and clinical features regarding signalment, type of epilepsy, severity, and etiological classification of epilepsy have not been established in dogs.

Therefore, the objectives of this retrospective study were as follows: to evaluate the prevalence of presumed PC in the MRI scan of a population of epileptic dogs, to describe the brain distribution of suspected PC changes, and to identify possible associations between the presence of PC and different epilepsy characteristics (ES type; etiology, severity, and time lapse between last ES and MRI scan).

Materials and Methods

Case selection criteria

Medical records of the Neurology Services of 4 referral Veterinary Hospitals (Ars Veterinaria Veterinary Hospital, Anderson Moores Veterinary Specialists, Animal BlueCare Veterinary Hospital, Canis Veterinary Hospital) from January 2016 to December 2019 were reviewed to identify dogs that had a diagnosis of epilepsy (idiopathic, structural, or unknown origin based on International Veterinary Epilepsy Task Force Classification [IVETF]) and on which MRI of the head had been performed. Dogs were included in the study if complete medical record and MRI report performed by a board-certified radiologist (ECVDI) or a board-certified neurologist (ECVN) were available and if diagnostic MRI images were available for review. Dogs with a diagnosis of reactive seizures were excluded.

Medical records review

For each patient eligible for study inclusion, information extracted from the medical record included signalment (age, breed, sex, and neutered status), ES type (focal or generalized—assigned as focal when only focal seizures had been visualized and assigned as generalized when at least 1 generalized seizure had occurred; this categorization was based on owner’s description of episodes or on video recording when available), severity of the last seizure episode (self-limiting, CSs, or SE according to IVETF definitions), time lapse between last ES and MRI scan (days), and etiological classification of epilepsy (idiopathic, structural, or unknown-origin epilepsy based on the IVETF definitions). For etiological classification of epilepsy, the most likely diagnosis was extracted from the medical record, considering MRI findings, CSF results, and clinical information including progression of disease when available.

Imaging

MRI was performed using a high-field 1.5-T scanner (Vantage Elan [Canon Medical Systems], Achieva [Philips Medical Systems], or MR-Signa Excite [General Electric Healthcare Systems]) or low-field 0.2- or 0.25-T scanner (Vet-MR; Esaote). T2W fast spin echo images were acquired in dorsal, sagittal, and transverse planes. All MRI studies were performed under general anesthesia. Dog positioning was dependent on protocols of each center. For dogs with clinically suspected idiopathic epilepsy, IVETF protocol recommendations were used. Additional sequences included fluid-attenuated inversion recovery (FLAIR), T2* gradient echo, and pre- and postcontrast with gadoteridol (Magnevist, ProHance, or Dotarem at a dosage of 0.1 mmol/kg of body weight, IV) T1W fast spin echo images. MRI images had been evaluated by a board-certified radiologist or a board-certified neurologist at the time of diagnosis. Where reports described PC, complete MRI was reviewed for the purpose of the study by one of the authors (PM, DS-M, SR, CF), following the same criteria. Parenchymal lesions observed on MRI were considered PC—rather than the cause of epilepsy or an incidental finding—when they showed the following MRI features: solitary or multiple intraparenchymal lesion(s) not confined to a vascular territory, hyperintense signal intensity related to the cerebral gray matter on T2W and FLAIR sequences and hypointense or isointense signal intensity on T1W images, no to mild mass effect, and no to mild contrast enhancement. MRI reports were retrospectively reviewed and the following information was extracted: presence or absence of signal changes interpreted to be most likely a consequence of ictal activity (PC group vs non-PC group); distribution of these changes; presence or absence of a brain lesion diagnosed as the cause of ESs (structural vs idiopathic or unknown-origin epilepsy); in case of structural epilepsy, side of the lesion and relationship with side of PC; and presumptive or main differential etiological diagnosis.

Statistical analysis

Statistical analyses were performed using statistical software (SPSS Statistics version 25.0; IBM Corp). Descriptive statistics of quantitative variables was carried out with median and interquartile range. Descriptive statistics of categorical variables were expressed as percentages. Categorical variables were analyzed by comparing proportions using Pearson’s χ2 or Fisher’s exact test. The relationship between a binary variable exposure and a quantitative response was analyzed with the Student-Fisher t test for independent samples and the nonparametric Mann-Whitney U test according to normality assessment.

Multivariable logistic regression was used to determine the association between PC (yes or no; dependent variable) and sex, type of ESs, seizure severity, time between last ES and MRI scan in days, and etiological classification of epilepsy. The multivariable model was constructed with a manual backward stepwise removal approach. Only variables with a value of P < 0.05 were retained. The predictive capacity of the models was estimated by the Nagelkerke square coefficient R. Receiver operating characteristic curves were configured to calculate cutoff points for discrimination between the presence and absence of PC.

Results

Animals

A total of 540 dogs from the 4 collaborating veterinary hospitals met the study inclusion criteria. Median age of these dogs was 7 years (range, 2.5 months to 18 years) and included 153 castrated males, 143 sexually intact males, 139 spayed females, and 105 sexually intact females. Breeds included mixed-breed dogs (n = 99), French Bulldog (62), Labrador Retriever (36), Chihuahua (31), Boxer (24), Yorkshire Terrier (23), Maltese (22), German Shepherd Dog (18), Golden Retriever (17), Miniature Schnauzer (15), English Cocker Spaniel (14), Border Collie (11), Pug (11), American Staffordshire Terrier (10), Beagle (9), Dachshund (9), English Bulldog (8), Miniature Poodle (7), Siberian Husky (7), and 57 other breeds represented by 1 to 5 dogs each.

From the total of enrolled animals, 67 dogs (12.4%) showed MRI features consistent with PC. Median age of these dogs was 7 years (range, 10 months to 15 years), and the dogs included 20 castrated males, 24 sexually intact males, 16 spayed females, and 7 sexually intact females. French Bulldog was the most common breed represented in the PC group (n = 14 [20.9%]). Other breeds included mixed-breed dog (11 [16.4%]), American Staffordshire Terrier (4 [6%]), Maltese (4 [6%]), Labrador Retriever (4 [6%]), Chihuahua (3 [4.5%]), Jack Russell Terrier (3 [4.5%]), Beagle (2 [3%]), English Cocker Spaniel (2 [3%]), Golden Retriever (2 [3%]), Siberian Husky (2 [3%]), German Shepherd Dog (2 [3%]), Yorkshire Terrier (2 [3%]), and 1 (1.5%) each of Andalusian Mouse-Hunting Dog, Boxer, Cavoodle, Collie, Coton de Tulear, Dalmatian, Dogo Argentino, Dogue de Bordeaux, Catalan Shepherd, American Pitbull Terrier, Irish Setter, and Dachshund.

No significant differences were observed between dogs with or without PC regarding breed (P = 0.151), sex (P = 0.118), and age (P = 0.375).

MRI features

In total, 67/540 dogs (12.4%) were reported to show MRI findings consistent with PC. Low-field (0.2 or 0.25 T) and high-field (1.5 T) MRI were used to study 192 and 348 dogs respectively, with 29 (15.1%) and 38 (10.9%) dogs showing presumed PC. No significant differences were observed for low- versus high-field MRI to detect PC (P = 0.158).

Lesions consistent with PC were limited to a single brain location (either unilateral or bilateral) in 35 of 67 (52.2%) dogs. Of these, the most common sites affected were the piriform lobe (14/35), hippocampus (12/35), and cingulate gyrus (4/35; Figures 13). In 32 of 67 (47.8%) dogs, presumed PC were multifocal, with 24 of 32 animals showing lesions at 2 different locations, 6 of 32 at 3 locations, and 2 of 32 at 4 locations. Piriform-hippocampus (9/32) and piriform lobe–temporal neocortex (8/32) were the most common combined sites affected. Additional details about location of PC are shown (Table 1).

Figure 1
Figure 1
Figure 1
Figure 1
Figure 1
Figure 1
Figure 1

Transverse T2-weighted (T2W; A), fluid-attenuated inversion recovery (B), T1-weighted (T1W; C), and T1W postcontrast (D) MRI images of the head, at the level of hippocampus, of a 3-year-old German Shepherd Dog that presented for cluster seizures. Notice the bilateral, symmetrical increased signal intensity of the hippocampus in panels A and B. Signal intensity changes are barely perceptible in T1W (C), and contrast enhancement is not observed (D). In the transverse T2W (E), and dorsal T2W MRI images (F), notice the bilateral, symmetrical increased signal intensity of the cingulate gyrus. All these images are consistent with postictal changes (PC). A presumptive diagnosis of idiopathic epilepsy was made.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.21.02.0088

Figure 2
Figure 2
Figure 2
Figure 2
Figure 2

Transverse T2W (A), T2* (B), T1W (C), and T1W (D) postcontrast MRI images of the head of an 11-year-old French Bulldog that presented for cluster seizures. An intra-axial lesion causing mass effect is visible in the right piriform lobe. It is hyperintense to the gray matter on T2W, hypointense on T1W, shows ring contrast enhancement, and signal voids on T2* compatible with intralesional hemorrhages. This lesion is consistent with an intra-axial neoplasia. On left piriform lobe, a T2W hyperintense and T1W hypointense area is observed, with minimal mass effect and no contrast enhancement, consistent with PC.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.21.02.0088

Figure 3
Figure 3
Figure 3
Figure 3
Figure 3

Transverse T2W (A) and fluid-attenuated inversion recovery (B) images at the level of the thalamus, dorsal T2W (C) MRI image dorsal to the corpus callosum, and dorsal T2W (D) MRI image at the level of the thalamus of a 2-year-old crossbred dog presented for cluster seizures, with a diagnosis of idiopathic epilepsy. Bilateral and symmetrical hyperintensities affecting cingulate gyrus and thalamus are identified in A through D. These lesions are consistent with PC.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.21.02.0088

Table 1

Brain locations of suspected postictal changes in 67 epileptic dogs.

Brain location No. (%) of dogs
Piriform lobe 14 (20.9)
Hippocampus 12 (17.9)
Piriform lobe, hippocampus 9 (13.4)
Piriform, temporal neocortex 8 (11.9)
Cingulate gyrus 4 (6.0)
Piriform lobe, hippocampus, thalamus 2 (3.0)
Temporal, parietal neocortex 1 (1.5)
Temporal neocortex 1 (1.5)
Thalamus, frontal lobe 1 (1.5)
Thalamus 1 (1.5)
Piriform lobe, thalamus 1 (1.5)
Piriform lobe, hippocampus, temporal neocortex 1 (1.5)
Piriform lobe, hippocampus, thalamus, basal nuclei 1 (1.5)
Piriform lobe, hippocampus, thalamus, cingulate gyrus 1 (1.5)
Piriform, frontal lobes, parietal neocortex 1 (1.5)
Piriform, cingulate gyrus 1 (1.5)
Parietal neocortex 1 (1.5)
Caudate nucleus 1 (1.5)
Hippocampus, cingulate gyrus, frontal lobe 1 (1.5)
Hippocampus, cingulate gyrus 1 (1.5)
Frontal lobe, parietal neocortex, corpus callosum 1 (1.5)
Corpus callosum, thalamus 1 (1.5)
Cingulate gyrus, corpus callosum 1 (1.5)
Internal capsule 1 (1.5)
Total 67 (100.0)

Regarding lateralization, bilateral distribution of PC was detected in 46 of 67 (69.2%) dogs, whereas unilateral left and right sided were described in 15 of 67 (22.4%) and 6 of 67 (8.9%) respectively. From the total of 27 dogs having a structural lesion and PC, 8 of 27 had a left-sided lesion, 10 of 27 a right-sided lesion, and 9 of 27 a bilateral lesion. Evaluation of possible correlation between side of the lesion in dogs with structural epilepsy and side of suspected PC did not disclose significant results (P = 0.213).

Repeat MRI scan was performed in 4 dogs showing PC. Two of them were diagnosed with structural epilepsy, and MRI scan was repeated 6 and 8 weeks after the initial MRI scan. Both cases were presumptively diagnosed with a neoplasia. In the follow-up MRI scan, increased volume of the structural lesion was observed, and resolution of the PC was only partial in both cases. The other 2 dogs with presumptive diagnoses of idiopathic and unknown-origin epilepsy had a control MRI scan 12 and 13 weeks later respectively. Complete resolution of PC was observed in the follow-up MRI scan in both cases.

Clinical features

In the PC population, 2 of 67 dogs (3%) presented focal ESs, and 65 of 67 dogs (97%) suffered at least 1 generalized ES. In the non-PC population, 43 of 473 dogs (9.1%) developed focal ESs, and 430 of 473 (90.9%) dogs presented generalized ESs. The difference in prevalence of PC between dogs with focal seizures and dogs with generalized seizures was not significant (P = 0.091).

With regard to ES severity, 202 dogs presented with CSs or SE, of which 40 (19.8%) had PC, while 338 dogs exhibited a self-limiting presentation, with 27 of them (8%) having PC. Twenty-seven of sixty-seven (40.3%) dogs in the PC group and 311 of 473 (65.8%) dogs in the non-PC group had suffered a self-limiting seizure in the last episode; 26 of 67 (38.8%) dogs with PC and 135 of 473 (28.5%) dogs without PC had CSs, and SE was reported in 14 of 67 (20.9%) dogs with PC and in 27 of 473 (5.7%) dogs without PC. On bivariable analysis, a significant difference (P < 0.001) was found, demonstrating a higher prevalence of PC in dogs that had suffered CSs or SE in the last ES episode.

Regarding time between last ES and MRI scan, median time was 1 day (range, 0 to 38 days) for dogs with PC and 4 days (range, 0 to 130 days) in dogs without PC. This was statistically significant (P < 0.001). The maximum time lapse between last epileptic seizure and MRI scan in which PC were observed was 38 days. When this timeframe was considered (0 to 38 days), prevalence of PC was 12.3%, similar to the general population. The receiver operating characteristic curves indicated that the optimal cutoff point when using the time between last seizure and MRI scan to discriminate between the presence or absence of PC was 2.5 days. When selecting the sample of cases with a time lapse of ≤ 2.5 days between last seizure and MRI scan, there was a total of 219 cases, with a prevalence of dogs showing PC of 18.3%, which was higher compared to the general population (12.4%).

With respect to etiological classification of ESs, idiopathic epilepsy was diagnosed in 21 of 67 (31.3%) dogs with PC and 167 of 473 (35.3%) dogs without PC, structural epilepsy was diagnosed in 27 of 67 (40.3%) dogs with PC and 240 of 473 (50.7%) dogs without PC, and, finally, unknown origin epilepsy was diagnosed in 19 of 67 (28.4%) dogs with PC and 66 of 473 (14%) dogs without PC. Dogs with unknown-origin epilepsy were more likely to have PC than were dogs with structural or idiopathic epilepsy (P = 0.010).

Within the group of structural epilepsy with PC, the most likely reported etiological category was neoplasia in 17 of 27 (63%) dogs, inflammatory infectious disease in 6 of 27 (22.2%), vascular disorder in 3 of 27 (11.1%), and degenerative disorder in 1 of 27 (3.7%). In dogs without PC, neoplasia was mainly suspected in 138 of 240 (57.5%) dogs, inflammatory infectious disease in 47 of 240 (19.6%), congenital anomaly in 23 of 240 (9.6%), vascular disorder in 12 of 240 (5%), traumatic brain injury in 3 of 240 (1.3%), degenerative disorder in 2 of 240 (0.8%), and undefined lesions not easily categorized in 15 of 240 (6.3%).

On multivariable analysis, the presence of CSs or SE versus self-limiting seizures was associated with a higher probability to detect PC (OR 2.39; 95% confidence interval, 1.33 to 4.30; P = 0.004). Dogs with unknown-origin epilepsy were more likely to have presumed PC than were dogs with structural epilepsy (OR 0.15; 95% confidence interval, 0.06 to 0.33; P < 0.001) or idiopathic epilepsy (OR 0.42; 95% confidence interval, 0.20 to 0.87; P = 0.019).

Discussion

The current study describes the prevalence of presumed PC in MRI scan in a large population of epileptic dogs. Correlations between clinical features of epilepsy and presence of suspected PC were also reviewed, which have not been previously reported in veterinary medicine. CSs or SE, diagnosis of unknown-origin epilepsy, and lower time from the last seizure to MRI acquisition were identified as predictors of PC. Furthermore, brain distribution of the suspected PC changes was described.

Lesions presumed to be a consequence of ESs, defined as PC or peri-ictal changes, are frequently identified in dogs and widely reported in human medicine.7,8,9 Recognizing observed MRI lesions as PC has important implications in diagnosis, treatment and prognosis of dogs with epilepsy. Transient PC may mimic other brain disorders such as inflammatory, vascular, or neoplastic, resulting in therapeutic and prognostic implications.

PC are suggested to be caused by cytotoxic and vasogenic edema. In MRI, they are identified as hyperintensities on T2W and FLAIR sequences occurring in areas of cortical gray matter and, less frequently, subcortical white matter, indicating an increase in brain water.8,10,11,16,24,25,26 Diffusion-weighted imaging, a functional MRI sequence based upon measuring the random Brownian motion of water molecules within a voxel of tissue,27 is considered one of the most sensitive methods to identify PC, showing areas of restricted diffusion and indicating the presence of cytotoxic edema.10,12,16 In 1 recent veterinary study22 in which DWI was performed in 19 dogs, changes in apparent diffusion coefficient values were variable, showing facilitative, restrictive, normal, or a mixture of diffusivity, probably reflecting time-dependent changes in neuronal metabolism associated with seizure activity.22

In humans, contrast enhancement after gadolinium administration may occur, either of the affected region or the leptomeninges. This could be explained by the hypermetabolic state at the site of PC, or as a consequence of vasodilation and possible blood-brain barrier dysfunction.10,24 In the veterinary literature, detailed description of PC MRI features is available, reporting T2W and T2-FLAIR hyperintense, T1W iso- and hypointense areas with mild contrast enhancement, and possible local mild mass effect.20,22,23 Characterization of signal features and contrast enhancement of suspected PC in each individual case were beyond the scope of the present study, as different institutions with different MRI scanners and protocols were included, impeding standardization of sequences, and a definitive diagnosis of PC could not be reached. Presence or absence of presumed PC in our study was recorded from the MRI reports, which had been performed by a board-certified radiologist or neurologist in the clinical setting, taking into account both MRI features and clinical information. In our opinion, this reflects the situation of everyday clinical practice.

Currently, the most accepted hypothesis to explain seizure-associated changes is the excitotoxicity theory.8,17,18,24 When ESs occur, oxygen and glucose metabolisms in brain cells increase, resulting in high cerebral blood flow but insufficient oxygenation. Compensatory mechanisms fail, and an anaerobic metabolism may appear with an excess production of lactic acid. In severe ESs, such as CSs or SE, a reduction of the energy in the form of adenosine triphosphate can occur. This energy depletion may lead to a secondary sodium/potassium pump fail and an increase of the cell’s permeability, with a massive influx of sodium and calcium ions and efflux of potassium ions, which produces swelling of glial cells and neurons, consistent with cytotoxic edema. In addition, intracellular calcium may cause cell death through apoptosis by different mechanisms and by its action on N-methyl-d-aspartate receptors, such as activation of proteases and phospholipases. On the other hand, and secondary to the excessive release of excitatory amino acids, such as glutamate or aspartate, there is an increase in the membrane ion permeability, inducing swelling of the extracellular space, consistent with vasogenic edema.24,28

In the present study, presumed PC were present in a single location in 52.2% of dogs, whereas 47.8% of dogs showed multiple locations. This is in accordance with the human literature, which reports both single and multiple lesions, which can appear distant from each other.9,10,17 In the veterinary literature, PC have been reported in the hippocampi, cingulate gyrus, caudate nuclei, thalamus, piriform, olfactory, frontal, temporal, and occipital lobes.20,21,22,23 In the current study, the most common sites affected by suspected PC were the piriform lobe, hippocampus, other areas of temporal neocortex, and cingulate gyrus. Other locations identified less commonly were pulvinar thalamic nuclei, parietal neocortex and frontal lobes, caudate nucleus, corpus callosum, and internal capsule. These findings are in accordance with a recent study,22 where hippocampus, cingulate gyrus, and piriform lobe were considered the most commonly affected sites. Some of the areas identified in the present study, such as corpus callosum or internal capsule, have not been previously described in veterinary medicine. In humans, PC distribution can be highly variable and may involve different cortical and subcortical areas.10,11 PC may occur in the region of the epileptic discharge or in distant structures, possibly reflecting a seizure propagation pathway.10 Temporomesial structures, such as hippocampus or pulvinar nucleus of the thalamus, are the most commonly affected areas,12 which is explained by their known involvement in seizure propagation.9,11,12 Other described locations are the splenium of corpus callosum, the insular cortex, the basal nuclei, the cerebellum, and the claustrum.10,11 PC distribution may be related to the susceptibility of certain structures to the effects of ESs and to the propagation pathway of the epileptic discharge, affecting distinct areas of the cerebrum.10 Basal nuclei are thought to be affected by PC because of their role in the electric propagation pathway, as well as their close connection with thalamo-cortical areas.10 Changes in white matter, such as corpus callosum or internal capsule, could be explained by abnormal electric activity in these tracts, with microvacuolization of the myelin being the most accepted theory to explain the signal changes in the white matter.25 However, the exact mechanisms of this phenomenon are not completely understood. In our study, localization as insular cortex, claustrum, or cerebellum was not identified. In addition, bilateral distribution of PC changes was viewed in the majority of dogs (69.2%), supporting the theory of seizure propagation. This finding is in accordance with a recent report, where the majority of dogs also showed a bilateral distribution of PC.

In human medicine, the range of PC is also wide in terms of morphology, extent, contrast enhancement, and time course. PC can be single or multiple, unilateral or bilateral, completely or partially reversible, enhanced or not after gadolinium administration, and with or without mass effect.7,10 This wide variability of presentation poses a broad differential diagnosis, including vascular, neoplastic, inflammatory infectious diseases, Creutzfeldt-Jakob encephalopathy, complicated migraine, posterior reversible encephalopathy syndrome, and metabolic encephalopathies.15,29 In veterinary medicine, such differential diagnoses have not been investigated in the literature, but it is reasonable to state that presence of T2W hyperintensities consistent with PC may represent a diagnostic challenge. Several studies investigating MRI accuracy in the differentiation of neoplastic, inflammatory, and vascular lesions are available, with variable results in respect to sensibility and specificity of MRI diagnosis.30,31 Such investigations have not been performed on suspected PC. On the other hand, some metabolic and toxic encephalopathies produce MRI changes in the brain that can be similar to PC (ie, bilateral symmetrical T2W hyperintensities of variable distribution).32 These lesions may also be reversible, hindering differentiation between PC and other metabolic derangements caused by the metabolic or toxic insult. Therefore, in the present study, the decision was made to exclude all those cases with a clinical suspicion of reactive seizures. Definitive diagnosis of a lesion as PC would require histopathological confirmation. However, investigation of PC confirmed by histopathology is difficult, as most dogs with suspected PC are not euthanized in the short time before resolution of lesions. This probably explains the almost absence of veterinary literature addressing PC in dogs. Alternatively, a follow-up MRI scan after seizure control, with no other treatment but antiepileptic drugs, might help differentiate between seizure-induced changes and a primary parenchymal abnormality, although economic issues and risks associated with general anesthesia for a follow-up MRI preclude repeating MRI in the majority of cases in the clinical setting, and decisions are most commonly based on clinical course.

In the present study, histopathology was not performed. In the previous veterinary report in dogs,20 histological examination of reversible PC was performed and showed mild to moderate cortical gliosis and neuronal loss in the hippocampus and neocortex, with hypertrophy and hyperplasia of astrocytes. These findings are in accordance with human studies,33,34 where the histological features are detected mainly in the hippocampus, showing neuronal loss and reactive astrocytes with prominent, darkly staining nuclei and abundant eosinophilic cytoplasm, consistent with cytotoxic edema. Moreover, the neuropil presented rarefication, consistent with vasogenic edema. In epileptic cats, bilateral lesions in the hippocampus and piriform lobe have been reported to be associated with feline hippocampal necrosis, which has been hypothesized to be a consequence of epilepsy and possibly associated with limbic encephalitis.35,36,37 However, these lesions are not reversible and correspond histopathologically to neuronal degeneration or necrosis that affects mainly the pyramidal cortical layer.

Reversibility of PC is a phenomenon highly studied in human medicine.10,11,15 Follow-up MRI shows total or partial resolution of PC lesions. Complete resolution supports the hypothesis that they are a consequence rather than the cause of the seizures. Incomplete resolution of PC could be explained through the presence of chronic atrophy and neuronal cell loss and gliosis, indicating the possibility of hippocampal sclerosis in some patients.8,10,11,38 Time between first and follow-up MRI showing resolution of PC is variable. In the veterinary literature, dogs were reported to have complete or partial resolution of lesions in a wide time lapse, ranging from 1 week to 10 months.20,22 However, the optimal timing for repeating MRI to visualize whether observed changes are reversible is currently unclear. In the present study, MRI scan was repeated in only 4 dogs with PC, with a time lapse of 6 to 13 weeks after the initial study. Partial resolution of PC was observed in the 2 dogs in which MRI was performed at 6 and 8 weeks, and complete resolution was observed in the 2 dogs that had the control MRI performed at 12 to 13 weeks after the initial study.

In veterinary medicine, published correlations between clinical features and the presence of suspected PC are lacking. In human medicine, main studied clinical parameters associated with PC include time between seizures and performance of MRI8,18,19,39, duration and severity of seizure activity8,10,11,12,18,25,40, seizure type10,11,12,18,41,42,43, etiological classification9, and correlations between the sides of structural lesion and the side of PC.17

In the present study, sex, age, and breed were not significantly associated with PC. The presence of CSs and SE was identified as a predictor of suspected PC. This result is in accordance with previous reports18,25,40,44 in human medicine. Results of 1 study22 published in dogs also indicate an increased probability of PC in dogs with CSs or SE, with 72% of dogs showing PC having CSs or SE. However, prevalence was not evaluated, as all of the dogs included showed PC. In the human literature, it has been postulated that severity of seizure is an important determinant of peri-ictal imaging abnormalities.8,10,11,12,18 The presence of cytotoxic edema is associated to longer seizure activity due to stimulation of anaerobic glycolysis during the ictal activity, provoking a failure in the energy metabolism.18,40 In addition, CSs and SE could cause hemodynamic changes and alteration of the leptomeningeal blood-brain barrier.44

The majority of dogs included in previous reports were diagnosed with idiopathic epilepsy.20,21,22,23 In our study, suspected PC were equally identified in dogs with idiopathic and structural epilepsy. However, etiological classification as unknown-origin epilepsy was a predisposing factor for the visualization of PC. This finding is challenging to interpret; in the absence of a structural lesion as the cause of seizures in dogs that are not expected to suffer from idiopathic epilepsy and are therefore diagnosed with unknown-origin epilepsy (ie, due to signalment), the reported lesions interpreted as PC may actually correspond to inflammatory, vascular, or neoplastic lesions that are indeed responsible for the seizure activity. It is not possible to completely rule this possibility out for some of the cases, as neither histopathology nor follow-up MRI was available in our study. However, it was thought to be unlikely, as all except 1 of the cases with both PC and epilepsy of unknown origin showed the most commonly described pattern of PC (ie, unilateral or bilateral hyperintense T2W lesions affecting piriform, temporal neocortex, hippocampus, or a combination of any of these locations). In human medicine, correlation between etiological cause and PC is controversial. Some studies7,12,19 show that symptomatic seizures were a risk factor for the development of PC, whereas other reports9,17 demonstrate that etiology of seizures was not significantly different between groups with and without PC. Interestingly and in accordance with our results, there is a study24 reporting PC in 8 patients, 6 of them with a diagnosis of cryptogenic seizures.

Timing between seizure events and the presence of PC is a clinical feature widely described in people.8,18,19 A negative association exists between the presence of PC and the time interval between cessation of seizures and MRI acquisition. In the present study, this correlation was also observed, as suspected PC were identified more often when MRI studies were achieved earlier after the epileptic event. In a previous report including only dogs with PC, MRI scan was performed < 48 hours after the last seizure in 79% of cases.22 Our data revealed an optimal cutoff of 2.5 days to discriminate the presence or absence of PC in MRI scan. This finding implies that if the MRI scan is carried out soon after the epileptic activity occurs, it would be more likely to detect PC, especially when CSs or SE occur. This is also supported by the fact that, when the sample of cases with a time lapse of ≤ 2.5 days between the last seizure episode and MRI scan was selected, the prevalence of dogs showing PC increased to 18.3%. This is valuable information in the clinical practice, as proximity of ESs could in some cases increase suspicion that a certain lesion corresponds to a peri-ictal change rather than an underlying cause for the seizure activity. Another interesting datum is that the maximum time lapse between seizure and observed PC in our study was 38 days.

In people, patients with focal seizures are predisposed to show PC on MRI in comparison with generalized ESs.10,11,12,18,41,42,43 In the present study, we did not find a significant correlation between type of ESs and presence of PC changes. A possible explanation is the low number of dogs in the focal ES group. Due to the retrospective nature of the study, it was decided to allocate dogs that had suffered both focal and generalized ESs in the generalized seizure group, to standardize the population, as seizure type classification was often based on the owner’s description of the episodes. Therefore, we cannot be certain whether some of the patients with generalized seizures had a focal onset with a secondary generalization or had also suffered focal ESs. Moreover, information about epilepsy semiology was extracted from the medical records, where differentiation between generalized and focal seizures was based either on video recordings or on the owner’s description, and there might be some rate of error in this categorization. In other research evaluating dogs with PC and suspected idiopathic epilepsy, 86% of the dogs presented generalized ESs.22 A prospective study including a more detailed description of type of seizure episodes and discriminating dogs with generalized, focal, and focal with secondary generalization would be necessary to investigate whether seizure type could also influence development of PC in dogs.

Limitations of the present study included its retrospective and multicenter nature. First, due to the retrospective nature, MRI protocols used in the different institutions were not standardized. Also, different protocols were performed depending whether the patient was expected to suffer idiopathic or structural epilepsy, based on IVETF recommendations.6 This could have especially influenced detection of changes in the hippocampus, as MRI protocols in dogs suspected to have idiopathic epilepsy are planned to optimize assessment of the hippocampus.6

Another limitation is that a systematic review of all the 540 MRI scans by the same investigator was not performed. Imaging reports were reviewed searching for a description of PC. It is therefore not possible to completely rule out that some cases showed PC that were not described in the imaging report. This would have resulted in underestimation of the reported prevalence.

On the other hand, DWI was not available in the majority of dogs. This sequence has been shown to be sensitive for the detection of PC in humans and has also been suggested for dogs.12,22 Therefore, it is possible that prevalence of PC in dogs was underestimated in our study. The main limitations were the lack of histopathology to confirm diagnosis of PC and the lack of follow-up MRI to confirm complete or partial reversibility of lesions. We cannot therefore completely rule out that some of the lesions categorized as PC did actually correspond to some other type of lesions. This is especially applicable to dogs with structural epilepsy. Neoplastic or inflammatory disorders involving the piriform lobe or other areas commonly affected by PC may be difficult to differentiate from PC in the clinical setting. However, we believe this reflects the clinical challenge of everyday practice when it comes to making an etiological diagnosis of epilepsy. Repeating MRI scan is always advisable in dogs where difficulties appear to distinguish between PC and brain structural lesions causing epilepsy. Due to economic restraints of owners and risks associated with general anesthesia, follow-up MRI is rarely performed in epileptic dogs, and clinical decisions are most commonly based on the dog’s clinical course. Future prospective studies evaluating follow-up MRI could improve our knowledge about the reversibility of PC.

In conclusion, the present study is the first to establish a prevalence of suspected PC in epileptic dogs. MRI lesions consistent with PC were present in dogs with idiopathic, structural, and unknown-origin epilepsy and were equally detected on high- and low-field MRI. Distribution was variable in the brain, with more frequent involvement of the piriform lobe, hippocampus, temporal neocortex, and cingulate gyrus. Analysis of the clinical factors related to the presence of suspected PC showed that they were more common in dogs with CSs or SE and in dogs with unknown-origin epilepsy. PC were also detected more often in patients who had undergone MRI more promptly after the last seizure. Prospective studies including a large number of cases confirmed by histopathology or follow-up MRI are needed to better characterize PC features in dogs.

Acknowledgments

No funding was received for this study. The authors declare that there were no conflicts of interest.

Presented in part (81 cases) as a poster presentation at the 31st Annual Symposium of the European Society of Veterinary Neurology, Copenhagen, September 2018.

The authors thank Drs. Sergio Moya and Natalia Martínez for supplying information for some of the cases.

References

  • 1.

    Kearsley-Fleet L, O’Neill DG, Volk HA, Church DB, Brodbelt DC. Prevalence and risk factors for canine epilepsy of unknown origin in the UK. Vet Rec. 2013;172(13):338.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Heske L, Nødtvedt A, Jäderlund KH, Berendt M, Egenvall A. A cohort study of epilepsy among 665,000 insured dogs: incidence, mortality and survival after diagnosis. Vet J. 2014;202(3):471476.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Berendt M, Farquhar RG, Mandigers PJJ, et al. International veterinary epilepsy task force consensus report on epilepsy definition, classification and terminology in companion animals. BMC Vet Res. 2015;11:182. doi:10.1186/s12917-015-0461-2

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Lee BI, Heo K, Kim JS, et al. Syndromic diagnosis at the epilepsy clinic: role of MRI in lobar epilepsies. Epilepsia. 2002;43(5):496504.

  • 5.

    De Risio L, Bhatti S, Muñana K, et al. International veterinary epilepsy task force consensus proposal: diagnostic approach to epilepsy in dogs. BMC Vet Res. 2015;11:148. doi:10.1186/s12917-015-0462-1

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Rusbridge C, Long S, Jovanovik J, et al. International Veterinary Epilepsy Task Force recommendations for a veterinary epilepsy-specific MRI protocol. BMC Vet Res. 2015;11:194. doi:10.1186/s12917-015-0466-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Grillo E. Postictal MRI abnormalities and seizure-induced brain injury: notions to be challenged. Epilepsy Behav. 2015;44:195199.

  • 8.

    Briellmann RS, Wellard RM, Jackson GD. Seizure-associated abnormalities in epilepsy: evidence from MR imaging. Epilepsia. 2005;46(5):760766.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Milligan TA, Zamani A, Bromfield E. Frequency and patterns of MRI abnormalities due to status epilepticus. Seizure. 2009;18(2):104108.

  • 10.

    Cianfoni A, Caulo M, Cerase A, et al. Seizure-induced brain lesions: a wide spectrum of variably reversible MRI abnormalities. Eur J Radiol. 2013;82(11):19641972.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Giovannini G, Kuchukhidze G, McCoy MR, Meletti S, Trinka E. Neuroimaging alterations related to status epilepticus in an adult population: definition of MRI findings and clinical-EEG correlation. Epilepsia. 2018;59(suppl 2):120127.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Chatzikonstantinou A, Gass A, Förster A, Hennerici MG, Szabo K. Features of acute DWI abnormalities related to status epilepticus. Epilepsy Res. 2011;97(1-2):4551.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Yaffe K, Ferriero D, Barkovich AJ, Rowley H. Reversible MRI abnormalities following seizures. Neurology. 1995;45(1):104108.

  • 14.

    Rao TH, Libman RB, Patel M. Seizures and ‘disappearing’ brain lesions. Seizure. 1995;4(1):6165.

  • 15.

    Silverstein AM, Alexander JA. Acute postictal cerebral imaging. Am J Neuroradiol. 1998;19(8):14851488.

  • 16.

    Mendes A, Sampaio L. Brain magnetic resonance in status epilepticus: a focused review. Seizure. 2016;38:6367.

  • 17.

    Kim SE, Lee BE, Shin KJ, et al. Characteristics of seizure-induced signal changes on MRI in patients with first seizures. Seizure. 2017;48:6268.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Goyal MK, Sinha S, Ravishankar S, Shivshankar JJ. Peri-ictal signal changes in seven patients with status epilepticus: interesting MRI observations. Neuroradiology. 2009;51(3):151161.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Requena M, Sarria-Estrada S, Santamarina E, et al. Peri-ictal magnetic resonance imaging in status epilepticus: temporal relationship and prognostic value in 60 patients. Seizure. 2019;71:289294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Mellema LM, Koblik PD, Kortz GD, LeCouteur RA, Chechowitz MA, Dickinson PJ. Reversible magnetic resonance imaging abnormalities in dogs following seizures. Vet Radiol Ultrasound. 1999;40(6):588595.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Viitmaa R, Cizinauskas S, Bergamasco LA, et al. Magnetic resonance imaging findings in Finnish Spitz dogs with focal epilepsy. J Vet Intern Med. 2006;20(2):305310.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Nagendran A, McConnell F, De Risio LR, et al. Peri-ictal magnetic resonance imaging characteristics in dogs with suspected idiopathic epilepsy. J Vet Intern Med. 2021;35(2):10081017.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Carletti B, Oliveira M, Wessmann A. Peri-ictal MRI abnormalities in the hippocampus and cingulate gyri in five dogs with epileptic seizures. J Vet Intern Med. 2020;34(6):3048. 32nd ESVN-ECVN Symposium abstract P106.

    • Search Google Scholar
    • Export Citation
  • 24.

    Kim JA, Chung JI, Yoon PH, et al. Transient MR signal changes in patients with generalized tonicoclonic seizure or status epilepticus: periictal diffusion-weighted imaging. AJNR Am J Neuroradiol. 2001;22(6):11491160.

    • Search Google Scholar
    • Export Citation
  • 25.

    Cole AJ. Status epilepticus and periictal imaging. Epilepsia. 2004;45(suppl 4):7277.

  • 26.

    Williams JA, Bede P, Doherty CP. An exploration of the spectrum of peri-ictal MRI change; a comprehensive literature review. Seizure. 2017;50:1932.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Hecht S, Adams W. MRI of brain disease in veterinary patients part 1: basic principles and congenital brain disorders. Vet Clin North Am Small Anim Pract. 2010;40(1):2138.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    McNamara JO. Cellular and molecular basis of epilepsy. J Neurosci. 1994;14(6):34133425.

  • 29.

    Hicdonmez T, Utku U, Turgut N, Cobanoglu S, Birgili B. Reversible postictal MRI change mimicking structural lesion. Clin Neurol Neurosurg. 2003;105(4):288290.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Wolff CA, Holmes SP, Young BD, et al. Magnetic resonance imaging for the differentiation of neoplastic, inflammatory, and cerebrovascular brain disease in dogs. J Vet Intern Med. 2012;26(3):589597.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Cervera V, Mai W, Vite CH, Johnson V, Dayrell-Hart B, Seiler GS. Comparative magnetic resonance imaging findings between gliomas and presumed cerebrovascular accidents in dogs. Vet Radiol Ultrasound. 2011;52(1):3340.

    • Search Google Scholar
    • Export Citation
  • 32.

    Sharma P, Eesa M, Scott JN. Toxic and acquired metabolic encephalopathies: MRI appearance. AJR Am J Roentgenol. 2009;193(3):879886.

  • 33.

    Chan S, Chin S, Kartha K, et al. Reversible signal abnormalities in the hippocampus and neocortex after prolonged seizures. AJNR Am J Neuroradiol. 1996;17(9):17251731.

    • Search Google Scholar
    • Export Citation
  • 34.

    Fountain NB. Cellular damage and the neuropathology of status epilepticus. In: Drislane FW, ed. Current Clinical Neurology: Status Epilepticus: A Clinical Perspective. Humana Press; 2005:181193

    • Search Google Scholar
    • Export Citation
  • 35.

    Pakozdy A, Halasz P, Klang A, et al. Suspected limbic encephalitis and seizure in cats associated with voltage-gated potassium channel (VGKC) complex antibody. J Vet Intern Med. 2013;27(1):212214.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Marioni-Henry K, Monteiro R, Behr S. Complex partial orofacial seizures in English cats. Vet Rec. 2012;170(18):471.

  • 37.

    Fors S, Van Meervenne S, Jeserevics J, Rakauskas M, Cizinauskas S. Feline hippocampal and piriform lobe necrosis as a consequence of severe cluster seizures in two cats in Finland. Acta Vet Scand. 2015;57(1):41. doi:10.1186/s13028-015-0127-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Cartagena AM, Young GB, Lee DH, Mirsattari SM. Reversible and irreversible cranial MRI findings associated with status epilepticus. Epilepsy Behav. 2014;33:2430.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Scott RC, Gadian DG, King MD, et al. Magnetic resonance imaging findings within 5 days of status epilepticus in childhood. Brain. 2002;125(pt 9):19511959.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Szabo K, Poepel A, Pohlmann-Eden B, et al. Diffusion-weighted and perfusion MRI demonstrates parenchymal changes in complex partial SE. Brain. 2005;128(pt 6):13691376.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Raghavendra S, Ashalatha R, Krishnamoorthy T, Kesavadas C, Thomas SV, K Radhakrishnan. Reversible periictal MRI abnormalities: clinical correlates and long-term outcome in 12 patients. Epilepsy Res. 2007;73(1):129136.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Huang YC, Weng HH, Tsai YT, et al. Periictal magnetic resonance imaging in status epilepticus. Epilepsy Res. 2009;86(1):7281.

  • 43.

    Di Bonaventura C, Bonini F, Fattouch J, et al. Diffusion-weighted magnetic resonance imaging in patients with partial status epilepticus. Epilepsia. 2009;50(suppl 1):4552.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Nakae Y, Kudo Y, Yamamoto R, et al. Relationship between cortex and pulvinar abnormalities on diffusion-weighted imaging in status epilepticus. J Neurol. 2016;263(1):127132.

    • Crossref
    • Search Google Scholar
    • Export Citation
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