Childs Nerv Syst DOI 10.1007/s00381-014-2387-6

ORIGINAL PAPER

Prevalence of resistant occipital lobe epilepsy associated with celiac disease in children Alper I. Dai & Aylin Akcali & Celal Varan & Abdullah T. Demiryürek

Received: 23 December 2013 / Accepted: 11 February 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Purpose Celiac disease (CD) is a chronic, inflammatory autoimmune disorder caused by intolerance to ingested gluten. Increased frequency of CD has been reported in occipital lobe epilepsy. The aim of the present study is to investigate the frequency of CD among children followed up due to epilepsy and diagnosed with epileptic activity in the occipital lobe in at least one electroencephalography (EEG) test. Methods For this research, 90 pediatric epilepsy patients with epileptic activity in the occipital lobe were enrolled in the study group, while the control group comprised of 100 healthy children. In addition to the EEG examination, tissue transglutaminase (tTG) antibody was determined on duodenal biopsy. Results None of the healthy children in the control group was positive in terms of the tTG antibody test used to scan CD. In the group with epileptic activity in the occipital lobe, two patients out of 90 were tTG antibody positive. The seroprevalence was 1/45 (2.22 %) in this group. These two patients were diagnosed with CD based on the endoscopic duodenal biopsy. In these patients, the seizures were uncontrollable through monotherapy. A. I. Dai (*) Department of Pediatric Neurology, Faculty of Medicine, University of Gaziantep, 27310 Gaziantep, Turkey e-mail: [email protected] A. Akcali Department of Neurology, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey C. Varan Department of Pediatrics, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey A. T. Demiryürek Department of Medical Pharmacology, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey

Conclusions Our results showed that the prevalence of CD is observed to be higher than the normal population among the patients with occipital lobe epilepsy. This type of seizure disorder seems to be more resistant to monotherapy, compared with other types of occipital epilepsy. Therefore, screening for CD is recommended in children with resistant epileptic activity in the occipital lobe. Keywords Celiac disease . Occipital lobe epilepsy . Prevalence . Resistant

Introduction Celiac disease (CD) is a multi-systemic condition that occurs due to hypersensitivity to the gluten contained in crops and is characterized by the inflammation in the intestinal mucosa and submucosa caused by the immune mechanisms in genetically predisposed individuals, frequently leading to malabsorption [13, 29]. Genetic, environmental, and immune factors all play a role in the development of CD. The prevalence and incidence of both clinically and serologically diagnosed CD increased in recent years [16, 29]. Although it usually manifests itself through gastrointestinal complaints, there is also a silent or asymptomatic form of the disease. Extragastrointestinal symptoms may become prominent with advancing age [4, 28]. The clinical symptoms tend to improve once gluten is excluded from the diet. The disease may also manifest itself with extraintestinal symptoms including neurological findings. A wide range of neurological symptoms including ataxia, epilepsy, and peripheral neuropathies is observed in CD. The concurrence of CD with epilepsy has been reported in consecutive studies within the last years, and this point has recently become prominent in the related literature [12, 28]. It is observed that the triggering factor in inflammatory events of the disease is the gliadin peptides [5]. Gliadin

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peptides deamidated by the tissue transglutaminase (tTG) enzyme initiate an autoinflammatory cascade through the stimulation of T-lymphocytes by the cytokines in the dendritic cells of the genetically predisposed individuals. The tTG antibody is generated against the tTG enzyme bonded with gliadin. The tTG antibody can be detected in the serum and the antibody levels may be observed to diminish through a glutenfree diet [8]. A wide range of neurological symptoms including predominantly ataxia, epilepsy, and peripheral neuropathies is observed in CD [4, 12]. Various neurological conditions such as polyneuropathy, migraine, myopathy, myoclonus, dementia, and encephalitis are manifestations of the disease observed in celiac patients [3]. Another important group of neurological conditions reported to be concurrent with CD is epilepsy. There is also evidence that individuals with CD appear to be at a moderately increased risk of epilepsy [19]. It is reported that especially patients with partial epilepsy with occipital paroxysm should be tested in terms of CD [4]. The aim of the present study is to investigate the frequency of CD among the patients followed up due to the diagnosis of epilepsy, in which at least one electroencephalography (EEG) examination has indicated epileptic activity in the occipital lobe.

Patients and methods Type and setting of the study This study was conducted at the Gaziantep University Hospital Pediatric Neurology Clinic between March 2013 and May 2013. For the purposes of the study, from among the epileptic patients being followed up, the ones in which epileptiform activity in the occipital lobe was observed in at least one EEG examination were selected. The retrospective analysis revealed that 90 patients were eligible for the study. The families of the patients were informed about the study. These patients were enrolled in the study after their parents/ legal guardians signed the informed consent form. The patient group also underwent physical examinations, and the findings were recorded in the patient follow-up forms. As the control group, 100 healthy children were included in the study after the signature of the informed consent forms by the parents/ legal guardians of the children. No EEG test was performed in the control group. Both groups were screened for the serum tTG antibody, which is used as a serologic marker for CD. For each subject included in any of the groups in this study, the IgG anti-tTG antibody was tested using the ELISA method from the serum samples. The patients who tested positive for the serum tTG antibody were referred to the Pediatric Gastroenterology Department of the Gaziantep University Hospital for the endoscopic biopsy to confirm the diagnosis of CD. Histopathologic changes obtained from the duodenal

biopsy material were interpreted according to the Marsh classification. The diagnosis of CD was determined by the IgG anti-tTG antibodies and by duodenal biopsy. The criteria used in the selection of the study group were (1) history of at least two unprovoked seizures with an interval of 1 month consistent with the diagnosis of epilepsy and (2) epileptic activity in the occipital lobe observed in at least one EEG. The exclusion criteria consisted of (1) cases of epilepsy due to febrile convulsions, (2) epileptic patients without epileptic activity in the occipital lobe, and (3) conventional (manifest) CD. The study was approved by the local Ethics Committee of the University of Gaziantep. Data collection from the patient group In compliance with the Gaziantep University Archive guidelines, the case files of the patients fulfilling the previously listed criteria were retrieved, and the patients’ histories, age, gender, types and forms of the seizures, demographic characteristics, laboratory results, EEG records, brain computed tomography, and magnetic resonance imaging (MRI) were studied. These data were summarized in individual forms for each patient entitled patient follow-up forms. The EEG examinations of the patients were performed using the Nihon Kohden-9100 Neofax brand 32-lead EEG device in the Pediatric Neurology Department. The test duration was 30 min for each patient, and recording has been made when the patient was awake or asleep. Uncooperative patients were sedated (with chloral hydrate 50 mg/kg/dose) before the EEG test. The EEGs obtained from all the patients were evaluated by the pediatric neurologist. Statistical analysis The Kolmogorov–Smirnov test was employed to test the normality of the distribution of the continuous variables. The independent group comparison of the variables with normal distribution was performed using Student’s t-test, while the Mann–Whitney U-test was used for the variables outside the normal distribution. The relationship between the categorical variables was tested through chi-square analysis. The ratio against the population was compared with the help of the one-sample Z-test. Descriptive statistics were expressed as frequency, percentage, or mean±standard deviation. The statistical analysis was performed using the SPSS statistical package software (SPSS Inc., version 11.5, Chicago, IL, USA), and statistical significance was based on a value of p0.05) and may have occurred by chance alone (Table 1). In the group with epileptic activity in the occipital lobe, the most frequently observed type of epilepsy based on patient history was symptomatic epilepsy. The group in which epileptiform activity was observed in the occipital lobe was classified based on the visual findings. Patients who had a history of oculomotor findings including ocular deviation were included in this subgroup, while in the other subgroups the symptoms were classified as transient loss of vision, motor arrest, or seeing rings. While 25.6 % of the patients had no symptoms, 48.9 % had oculomotor findings, 4.4 % had transient loss of vision, and 20 % had motor arrest. In the group where epileptic activity in the occipital lobe was observed, the classification of the seizure types pointed out generalized tonic–clonic convulsions as the most frequently observed type of seizure with a ratio of 43.3 %. Other frequently observed seizure types were generalized seizures (23.3 %), complex partial seizures (12.2 %), and simple partial seizures (2.2 %). The patient group was inquired about concomitant diseases. Among these patients, 34 % had no concomitant diseases, while 16.5 % had mental retardation as the most frequent concomitant disease, followed by psychosocial mental motor retardation in 15.6 %. No calcifications in the occipital

lobe were observed in any of the computed tomography scans of the brain. Among the brain MRIs, 52.2 % were observed to be normal. The patients were also evaluated regarding the medical treatment they received. The most frequently used drugs were observed to be oxcarbamazepine and valproic acid. The other drug treatments included levetiracetam, phenobarbital, vigabatrin, topiramate, clonazepam, lamotrigine, and carbamazepine. In this group, we have also classified the patients according to the treatment modality as monotherapy or polytherapy. Patients who had received a minimum of three drugs during an appropriate period of time and in an adequate dose as monotherapy before a second drug was added to the treatment were included in the polytherapy group. The ratio of those receiving monotherapy and polytherapy were found to be similar in this group (Table 1). Both patients with the tTG antibody positive in the present study were in the symptomatic epilepsy subgroup and were treated with antiepileptic drugs (oxcarbamazepine and valproic acid). These patients had mental retardation, experienced visual symptoms, and had a right deviation in the eyes in one case, while the another complained from motor arrest (Table 2). The first patient with a positive tTG antibody was a 10year-old female patient who was being followed up at the Gaziantep University Hospital Pediatric Neurology Clinic due to symptomatic epilepsy. She had her first seizure at the age of 4. Patient history revealed mild mental retardation. She did not have any seizures during the last 2 years. Regarding the type of the seizures, she had a history of generalized tonic–clonic seizures. When the visual symptoms during the seizures were inquired, motor arrest was reported. The patient had no complaints related to the gastrointestinal system. When the family history was investigated, no kinship was observed between the parents. No one in the family had a history of epilepsy. The physical examination revealed her height and weight percentiles as 10 %. The neurological examination was normal. Her biochemical values in the laboratory tests were within normal limits and no anemia was detected in the complete blood count. Her MPV value was 9.3 fl. Her brain MRI was also normal (Fig. 1). The EEG recorded an epileptic activity at a frequency of 3 Hz/s indicating spikes and slow wave complexes in the bilateral occipital lobes and predominantly in the right hemisphere (Fig. 1). When the tTG antibody was found positive, the patient underwent a duodenal endoscopic biopsy in the Pediatric Gastroenterology Department of the Gaziantep University Hospital. Since the sample assessed in the pathology department was consistent with Marsh 3 (villous atrophy), the patient was diagnosed with CD (Fig. 1). The patient was started a on a gluten-free diet. The second patient with a positive tTG antibody was a 3years-and-6 month-old male patient who was also being followed up at the Gaziantep University Hospital Pediatric Neurology Clinic due to symptomatic epilepsy. He had his

Childs Nerv Syst Table 2 Distribution of the tTG antibody according to the type of the epilepsy, visual symptoms, and the antiepileptic mono- or polytherapy

tTG

History

Treatment regimen Monotherapy

Negative

Primary epilepsy

Symptomatic epilepsy

Positive

Symptomatic epilepsy

Visual symptoms

Total Visual symptoms

Total Visual symptoms Total

first seizure when he was 4 months old. Patient history revealed that he had mental retardation and was followed up by the pediatric psychology outpatient clinic due to attention deficit and hyperactivity disorder. He has been seizure-free for the last 15 months. Regarding the type of the seizures, he had a history of generalized tonic–clonic seizures. When the visual symptoms during the seizures were inquired, deviation in the eyes to the right was reported. The patient had no complaints related to the gastrointestinal system. When the family history was investigated, no kinship was observed between the parents. No one in the family had a history of epilepsy. The physical examination revealed his height and weight percentiles as 3 %. The neurological examination was normal. His biochemical values in the laboratory tests were within normal limits, but the complete blood count pointed out an anemia (Hb, 11.3 g/dl). His MPV value was 8.3 fl. His brain MRI was also normal (Fig. 2). The EEG recorded an epileptic activity indicating sharp waves with occasional spikes and slow wave complexes in the bilateral occipital lobes and predominantly in the right hemisphere (Fig. 2). Since the sample assessed in the pathology department was consistent with Marsh 3, the patient was diagnosed with CD (Fig. 2). The patient was started a on a gluten-free diet.

Discussion We observed that the biopsy-confirmed CD prevalence was 1/45 among the patients with antiepileptic activity in the occipital lobe. None of the 100 healthy children enrolled as controls were positive for the tTG antibody. Our study has included patients with idiopathic and symptomatic epilepsy

Total

Polytherapy

None

7

1

8

Oculomotor Transient loss of vision Motor arrest

10 2

8 0

18 2

3 22 5 12 1

2 11 10 13 1

5 33 15 25 2

4 0 22

8 1 33 1 1 2

12 1 55 1 1 2

None Oculomotor Transient loss of vision Motor arrest Seeing rings Oculomotor Motor arrest

where epileptic activity was detected in the occipital lobe. Two patients who were found to be positive in our study were already followed up with the diagnosis of symptomatic epilepsy. Since various systemic symptoms may accompany the gastrointestinal symptoms in CD, it is accepted as a multisystemic disease. The majority of the celiac cases manifest themselves with nonspecific signs and symptoms after infancy. The subgroup of celiac cases diagnosed based on these nonspecific symptoms is called atypical CD. Since genetic and environmental factors play a role in its pathogenesis, the prevalence of the disease around the world shows geographical differences. After the seroprevalence tests were developed during the 1980s, the prevalence rates of the disease rose from 0.1 to 1 %. Studies conducted in Europe in recent years have observed prevalence rates varying from 1/80 to 1/550. Also in our country, the observed prevalence rates are similar to Europe. In the largest-scale study conducted by Dalgic et al. [7], the prevalence among schoolchildren between the ages of 6 and 17 was found as 1/212. In a research conducted in Erzurum, a city located in Eastern Anatolia, the study group was formed with 1,263 healthy schoolchildren, and the prevalence based on biopsies was observed as 1/158 [10]. The neurological manifestations of CD are various. Although less commonly than the adults, various neurological diseases, including predominantly epilepsy, have been reported during childhood [18]. Other neurological diseases observed concurrently with CD during childhood can be listed as cerebellar ataxia, peripheral neuropathy, myositis, neuromyotonia, myasthenic syndrome, cerebral calcification, myelopathy, and dementia [3, 4, 12, 13]. There are other

Childs Nerv Syst Fig. 1 a EEG recording of the first patient with an epileptic activity in the occipital lobe. The EEG shows an epileptic activity at a frequency of 3 Hz/s, indicating spikes and slow wave complexes in the bilateral occipital lobes and predominantly in the right hemisphere. b Duodenal biopsy sample of the first epileptic patient positive for tTG antibody with Marsh 3b histological lesion. Original magnification×200. c The brain MRI of the first epileptic patient

Childs Nerv Syst Fig. 2 a EEG recording of the second patient with an epileptic activity in the occipital lobe. The EEG shows an epileptic activity indicating sharp waves with occasional spikes and slow wave complexes in the bilateral occipital lobes and predominantly in the right hemisphere. b Duodenal biopsy sample of the second epileptic patient positive for tTG antibody with Marsh 3b histological lesion. Original magnification×200. c The brain MRI of the second epileptic patient

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studies suggesting that the neurological diseases and complications are immune-mediated. Demonstration of the antiganglioside antibodies in patients with neurological symptoms [34] and the accumulation of IgA antibodies in the cerebral parenchyma of the patients with active CD also support this hypothesis [23]. Besides the tTG antibody test, the antiendomysial antibody and anti-gliadin antibody tests are also used to scan CD. Although the sensitivity and specificity of the tTG IgA antibody is especially high, it may give false positive results in case of the lack of IgA. Testing for tTG IgG may reveal undiagnosed occult CD due to coincidental IgA deficiency [33]. The WHO has recommended the use of tTG to screen for CD in developing countries. We have also used the highly sensitive and specific tTG IgG antibody as a scanning method among the specific epilepsy group enrolled in this study. The most frequently reported concurrent disease to celiac is epilepsy. The prevalence of CD in epileptic patients is two to three times higher than the general population, and although it is generally accepted as approximately 3–6 %, there are different results about the frequency of CD among epileptic patients. Ludvigsson et al. [19] reported that CD was associated with a 1.43-fold increased risk of epilepsy. Fois et al. [11] have observed the frequency of CD in epileptic children as 1/87. In another study by Labate et al. [17], where 72 pediatric idiopathic partial epileptic patients were assessed, the frequency was observed as 2.7 %. In a large-scale study by Pratesi et al. [24], where 119 pediatric and 136 adult epileptic patients were studied in comparison to 2,034 healthy children and 2,371 healthy adults as the controls, the frequency of CD confirmed through the antiendomysial antibody IgA scan and small intestinal biopsy was found as 1/127 in epileptic patients, while it was 1/293 in the control group. It is a known fact that the frequency of occipital lobe epilepsies and especially of epileptic activity resulting from the occipital lobe in the EEG is increased among patients with CD [2]. Sammaritano et al. [30] have described the concurrence of CD, epilepsy, and calcification in the occipital lobe for the first time in 1988. Later, this condition has come to be known as the CEC syndrome, referring to CD, epilepsy, and occipital lobe calcification. The CEC syndrome is a focal or complex partial type of epilepsy usually originating from the occipital lobe. There are only limited reports in the literature about direct screening for CD in children with epileptic activity in the occipital lobe. In a study conducted in our country, Dursun et al. [9] have observed the frequency of tTG IgA positivity as 4.7 % and the prevalence of biopsy-confirmed CD as 1.17 % among 170 epileptic children. In the first celiac disease prevalence study in Turkey, the total seropositivity was found to be 0.87 % [10]. In the present study, the patient group demonstrated an increased number of concomitant diseases (66 %). Mental retardation was the most frequent concomitant disease. It has

been reported that the prevalence of celiac disease is higher in children with Down syndrome than the other autoimmune conditions. A sixfold increased risk of CD in individuals with Down syndrome has been reported [20]. Cogulu et al. [6] have demonstrated 6.4 % antiendomysial antibody positivity with biopsy-proven villous atrophy in a Turkish Down syndrome population of 47 individuals. Therefore, it is likely that additional diseases could have an influence on the slightly higher incidence of CD compared with the controls in our study. Early weaning from breastfeeding is an important triggering factor for the development of CD [15]. In infants, ingesting gluten-rich foods during the first 3 months of life—the critical period—is a factor triggering the disease [21]. It has also been reported during the 1950s that the longer the infant is nursed, the later the onset of CD is observed. When breastfed infants are introduced gluten between the fourth and sixth month of life, they might be developing an oral tolerance. The mental retardation we observed in the etiology of the two symptomatic epileptic patients with CD in our study group may have triggered the CD along with insufficient intake of breast milk and early exposure to gluten. MPV has been recognized as an inflammatory marker in various conditions including celiac disease [25] and epilepsy [22]. Ozaydin et al. [22] compared children with simple and complex febrile seizure groups and found that MPV of complex febrile seizure was significantly lower than that of simple febrile seizure group. There was no healthy control group in that study. However, a healthy control group was used in our study, and we have found that the MPV value in the group with epileptic activity in the occipital lobe was higher than the control group. The underlying reason for this increase in MPV is not clear, but it may be a reflection of ongoing inflammation. Clinical and experimental evidences support the hypothesis that brain inflammatory processes might represent a key mechanism in the pathophysiology of seizures and epilepsy [25–27, 32]. Increased levels of proinflammatory cytokines, such as interleukin-6 (IL-6) [1], may be responsible for high MPV levels in patients with epilepsy. Carbamazepine, an antiepileptic drug, may cause an inflammatory reaction within hours, with increased levels of serum IL-6 [14]. Moreover, a significant positive correlation between carbamazepine dose and mean platelet volume was demonstrated in epileptic patients [31]. In conclusion, our study showed that the prevalence of CD was 1/45 (2.22 %) among the pediatric patients diagnosed with epilepsy, in which epileptic activity is observed in the occipital lobe through EEG. It should be pointed out that increased incidence of CD in occipital epilepsy patients was not statistically significant in the present study and may have occurred by chance alone. Since CD is a serious disease and early recognition with immediate dietary alteration may reduce long-term consequences, it is recommended to screen for CD in children with occipital epilepsy, especially if they are

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not responsive to monotherapy. It is, however, clear that further epidemiological studies are required if this association is to be definitively clarified.

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Prevalence of resistant occipital lobe epilepsy associated with celiac disease in children.

Celiac disease (CD) is a chronic, inflammatory autoimmune disorder caused by intolerance to ingested gluten. Increased frequency of CD has been report...
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