LIETUVOS SVEIKATOS MOKSLU UNIVERSITETAS FACULTY OF MEDICINE
RADIOLOGY DEPARTMENT
Value of CT in diagnostics of epileptogenic findings
Table of Contents ABSTRACT ……… 4 ABBREVIATIONS ………. 5 1. INTRODUCTION ……….. 6 1.1. Definition ………. 6 1.2. Epilepsy types ……… 6 1.3. Seizure triggers ………. 7
1.4. Importance of neuroimaging in epileptic patients ……….. 8
2. MATERIAL AND METHODS ………. 8
2.1. Computer Tomography ……….. 8
2.2. Magnetic Resonance Imaging ……… 9
2.3. Electroencephalography ……… 9
2.4. Positron Emission Tomography ……… 9
2.5. Single photon emission computed tomography (SPECT) ……… 9
3. RESULTS ……… 10
4. DISCUSSION ……… 18
5. CONCLUSION ………. 19
INDIVIDUAL DEVELOPMENT PLAN FOR THE FINAL MASTER’S THESIS
Student: Guillermo Fernandez Diaz
Group: 36, Course: 6th year of the Medical Integrated Master’s Study Program.
Duration of Master’s studies: 2014 to 2021 Supervisor: Tomas Budrys
Department: Radiology
Title of thesis in English: Value of CT in diagnostics of epileptogenic findings.
Title of thesis in Lithuanian: KT tyrimo reikšmė diagnozuojant epileptogeninius radinius. Abstract of the thesis: Epilepsy is a common neurological disorder with diverse etiologies. Neuroimaging plays an important role workup of patient with epilepsy. It helps to identify brain pathologies that require specific treatment; and also, in formulating syndromic and etiological diagnoses so as to give patients and their relatives an accurate prognosis.
Aim: To find the best imaging technique for epilepsy patients to find the cause of epilepsy and find an accurate treatment.
Objectives:
1) Abnormalities in patients with epilepsy found in EEG, CT, MRI, SPECT and PET. 2) Compare the efficacy between CT, MRI in patients with epilepsy.
Value of CT in diagnostics of epileptogenic findings: A literature review and clinical considerations.
ABSTRACT
Objectives: To search for abnormal findings in CT, MRI, EEG, SPECT and PET of patients with epilepsy; To compare the efficacy between CT and MRI in PWE.
Abstract: Epilepsy is a common neurological disorder with diverse etiologies. Neuroimaging plays an important role workup of patient with epilepsy. It helps to identify brain pathologies that require specific treatment; and also, in formulating syndromic and etiological diagnoses so as to give patients and their relatives an accurate prognosis.
Refractory epilepsy prevalence rate may be as high as 80-90/100.000 in general population. Identification of lesions often helps in managing refractory epilepsies more effectively. Patients with medically refractory epilepsy often have a structural brain abnormality that may be amenable to surgery.
Low field MRI is superior to modified CT in demonstrating subtle structural lesions of the temporal lobe. Temporal lobe epilepsy is the most common form of epilepsy encountered and is often refractory to drug therapy.
Functional imagings are used for pre-surgical work-up of refractory epilepsy cases with an aim to identify the epileptogenic focus and to delineate functional areas nearing the focus. Temporal lobectomy is increasingly recognised as an effective treatment, giving good results in 70-80% of patients, with low mortality.
While only EEG provides specific diagnostic information, the focus definition is poor on CT scans and generally good but less consistent in MRI.
ABBREVATIONS
• PWE – Patients with epilepsy
• CT – Computerized tomography
• MRI – Magnetic Resonance Imaging
• EEG – Electroencephalogram
INTRODUCTION
Epilepsy is a common neurological disorder that causes unprovoked, recurrent seizures. A seizure is a sudden rush of electrical activity in the brain. A mild seizure may be difficult to recognize, it can last a few seconds during which you lack awareness. Stronger seizures can cause spasms and uncontrollable muscle twitches [1], and can last a few seconds to several minutes. During a stronger seizure, some people become confused or lose consciousness. Afterward epileptic patients may have no memory of it happening
Types of epilepsy: [2]
• Generalized: Seizures produced by widespread abnormal electrical impulses present throughout the entire brain.
o Generalized tonic-clonic. (Grand Mal) The patient loses consciousness and usually collapses. The loss of consciousness is followed by generalized body stiffening (called the "tonic" phase of the seizure), then by violent jerking (called the "clonic" phase of the seizure), after which the patient goes into a deep sleep (called the "postictal" or "after-seizure" phase). During grand-mal seizures, injuries and accidents may occur, such as tongue biting and urinary incontinence.
o Absence. Brief loss of consciousness (just a few seconds) with few or no symptoms. The patient typically interrupts an activity and stares blankly. These seizures begin and end abruptly and might occur several times a day. Patients are usually not aware that they are having a seizure, but may have a feeling of "losing time."
o Myoclonic. Sporadic and brief jerking movements, usually on both sides of the body. Patients sometimes describe the jerks as brief electrical shocks. When violent, these seizures might result in dropping or involuntarily throwing objects.
o Clonic. Repetitive, rhythmic jerking movements that involve both sides of the body at the same time.
o Tonic. Muscle stiffness and rigidity.
o Atonic. Consist of a sudden and general loss of muscle tone, particularly in the arms and legs, which often results in a fall.
• Partial (sometimes referred to as focal or localized): Seizures produced by electrical impulses that generate from a relatively small or "localized" part of the brain (referred to as the focus).
o Simple partial. (awareness maintained) Simple partial seizures are further divided into four groups according to the nature of their symptoms:
§ Motor. Motor symptoms include movements such as jerking, stiffening, muscle rigidity, spasms, and head-turning.
is used to describe sensory symptoms that are present only (and not motor symptoms).
§ Autonomic. Autonomic symptoms most often involve an unusual sensation in the stomach termed "gastric uprising".
§ Psychological. Psychological symptoms are characterized by various experiences involving memory (the sensation of deja vu), emotions (such as fear or pleasure), or other complex psychological phenomena. o Complex partial. (awareness impaired) Includes impairment of awareness. Patients seem to be "out of touch," "out of it," or "staring into space" during these seizures. Symptoms may also involve some complex symptoms called automatisms. Automatisms consist of involuntary but coordinated movements that tend to be purposeless and repetitive. Common automatisms include lip smacking, chewing, fidgeting, and walking around.
o Partial seizure with secondary generalization. A partial seizure that evolves into a generalized seizure (typically a generalized tonic-clonic seizure).
Seizures may last as long as a few minutes.
Some people are able to identify things or situations that can trigger seizures. Identifying triggers isn’t always easy. A single incident doesn’t always mean something is a trigger. It’s often a combination of factors [3] that trigger a seizure. A few of the most commonly reported triggers are:
• Lack of sleep • Illness or fever • Stress
• Bright lights, flashing lights, or patterns • Caffeine, alcohol, medicines, or drugs
Neuroimaging plays an important role workup of patient with epilepsy. It helps to identify brain pathologies that require specific treatment; and also, in formulating syndromic and etiological diagnoses so as to give patients and their relatives an accurate prognosis.
Identification of these lesions often helps in managing refractory epilepsies more effectively. Functional imagines are used for pre-surgical work-up of refractory epilepsy cases with an aim to identify the epileptogenic focus and to delineate functional areas nearing the focus.
MATERIAL AND METHODS
The inclusion criteria for the study were a definite clinical diagnosis of the temporal lobe epilepsy and intractability. The form required both the absence (stare combined with impaired awareness and responsiveness), and features of temporal lobe involvement in the aura, such as deja vu, or in the seizure itself, such as automatism.
The latter required that seizure control be unsatisfactory despite optimal drug treatment. "Unsatisfactory" seizure frequency in this study ranged from one per fort night to five per day. The patients had all been tried on 3 major anticonvulsant drugs with unsatisfactory results.
We compared the abnormal findings that were detected by several imaging modalities.
All the imaging studies were reviewed by a certified neuroradiologist with at least 10 years of relevant experience.
The results were obtained by the investigations of different studies (in total 6), in which, the patients with refractory epilepsy underwent to several neuroimaging techniques. Those studies are mentioned in references at the end of this Literature review.
2.1 CT
Computerized tomography (CT) scan uses ionizing radiation and can generate excellent hard tissue imaging contrast with moderately good soft tissue resolution [4]. CT scan has a number of advantages like lower cost, ready accessibility, scan speed, etc...; which provide a relatively reliable imaging modality for most patients. In addition, new generation CT scanners can generate an image of the brain in seconds.
Although the use of CT for epileptic patients has reduced with availability of MRI, CT is still the imaging of choice for these patients under certain conditions. CT can accurately detect hemorrhage, infarcts, gross malformations, lesions with underlying calcification, and large tumors. Although CT is often of secondary or adjunctive importance.
Equivocal or borderline abnormalities were excluded and, in particular, atrophy was diagnosed only if moderate or severe. In all cases tumors and arteriovenous malformations were confirmed by angiography and/or operation.
2.2 MRI
As a rule, transaxial MR images were obtained. However, whenever necessary for better demonstration of the lesion, MR scanning was performed in coronal or sagittal planes as well.
MR was considered "positive" when an increased signal intensity was noted on the T2-weighted images when compared with the signal from the opposite hemisphere or when a mass was detected. Although structural lesions with very intense signal (long T2 relaxation time) were thought more likely to be intrinsic neoplasms, and foci with a less intense signal were thought more likely to be mesial sclerosis or gliosis.
All the MRI were performed using the standard protocol for epilepsy.
2.3 EEG
Sixteen-channel recordings were performed using scalp electrodes placed according to the 10/20 system and sphenoidal electrodes according to Ives and Gloor [5]. Both serial and average reference derivations were obtained with the patients awake and asleep.
EEG was performed routinely; electrophysiologic studies were supplemented by 3-to-7-day hospitalizations. Simultaneous EEG recording so that seizures could be detected and recorded during sleep as well as during waking hours. An EEG was considered positive when epileptiform activity was noted.
2.4 PET
anxiety, short Teflon catheters were inserted into an antecubital vein for injection and into a dorsal vein of the contralateral hand that was subsequently kept in a temperature-controlled water bath at 44°C for blood sampling [6].
Patients were then placed comfortably on a reclining chair, with their head inside the gantry of a four-ring Scanditronix PC 384 positron camera, requested to keep their eyes closed [7] until the end of the study, and given a rapid intravenous bolus injection of 180MBq 2-(18F) fluoro-2-deoxy-D-glucose (FDG) in 5ml sterile non-pyrogenic, normal saline solution.
Concurrently, recordings were started: seven equally spaced, 11-mm-thick slices from the canthomeatal line to 82 mm above and parallel to it were simultaneously scanned for 40min at consecutive intervals, gradually increasing from 1 to 5 min. All measured radioactivities were corrected for decay before they were entered in any model equation. Activity images recorded 30-40 min and 40-50 min after injection were transformed into quantitative metabolic maps according to the normalization procedure.
All metabolic images were analysed by visual inspection. Furthermore, for topography-related statistical analyses of regional metabolism, a comprehensive set of regions of interest (ROI) was outlined on all functional images by means of an interactive FORTRAN program in connection with the computer's image display system. Briefly, after the outer brain contour had been determined [8] on a tomographic image by edge-finding, generous raw region contours were automatically placed relative to that outer contour, one after the other, according to predefined geometrical standard parameters. Within each of these raw regions, the final subregion of interest was marked so as to cover all pixels with an activity above a chosen proportionate level.
2.5 SPECT
Single photon emission computerized tomography (SPECT) is a nuclear medicine imaging method that allows for the quantitative and qualitative evaluation of regional cerebral perfusion. It is not indicated in most of the patients with epilepsy but has an important role in presurgical evaluation of refractory epilepsy patients. The use of SPECT in epilepsy stems from the known association of seizures with increased ictal regional cerebral perfusion or interictal decrease in perfusion [9-10].
Cerebral SPECT was performed 10-30 min after i.v. injection of (99mTc)-hexamethylpropyleneamineoxime (Tc-HMPAO), using a rotating scintillation camera (Gammatome T9000/ CGR, 64 single scans per full rotation).
RESULTS
secondarily generalized seizures. In the overall group with abnormal scans (N = 51). In 39 of 51 cases the CT abnormality was thought to be etiologically related to the seizures and in 25 of these cases the finding on CT led to a surgical or specific medical.
Besides, in other studies, CT was complemented by EEG, MRI, PET and SPECT [Stefan, H., Pawlik, G., Böcher-Schwarz 1987]. In which 10 patients were researched. EEG demonstrated constant, non-specific, unilateral focal activity. Six patients had unilateral (Fig. 1), the other four bilateral interictal epileptic signs. A distinct inferior mesial onset of ictal EEG changes was found in four patients; another four exhibited ictal lateralization at onset (Fig 2); one patient showed alternating lateralization, and in another one no clear ictal EEG onset could be distinguished. Ictal and interictal findings agreed with respect to the side of the focus in seven cases. In two patients interictal focal signs occurred on both hemispheres, while ictal onset indicated a single side. Two patients showed no evidence of lateralization, either ictal or interictal.
Fig.1 Fig.2
Fig. 3
Table 1. Location and other characteristics of abnormalities detected by imaging methods in Stefan, H., Pawlik, G., Böcher-Schwarz 1987.
Patient CT MRI SPECT PET
1 Hippocampus
right Hypoperf. temp. - mesial right?
Hypomet. hippoc. > temporal right >> infer, frontal right
2 Uncus
hippoc, left Hypoperf. temp. left Hypomet. hippoc. > temporal left
3 Hyperperf.
temp. right Hypomet. pole and mesial part of temp. lobe (incl. hippoc.) right
4 Anter.
hippoc, right Hypoperf. temp. mesial right?
Hypomet. uncus and temp. pole > temp., infer, frontal right
5 Hippocampus
fight Hypoperf. temp. right a: Hypomet. uncus > pole right b: Hypomet.temp. - pariet.-occip, right
6 Insula
right Middle temp. right a: Hypomet. posterior inferior part of temp. lobe right b: Hypomet. uncus, pole right
7 Hyperperf.
anter, temp. right?
a: Hypomet. pole and uncus right b: Hypomet. operculum, insula right
8 Pole
right Anter. temp. right pariet, left?
Hypoperf. temp. occip, left
a: Hypomet. mesial pole right b: Relative hypermet, lat. pole > posterior part right
9 Infer. temp.
fight Hypoperf. temp. right, pariet.-occip, left
a: Hypomet. hippoc., pole right b: Hypomet.hippoc., pole left
10 Pole left Pole left Hypoperf. front. - temp. left and right?
a: Hypomet. uncus hippoc., pole right
PET always revealed unilateral (8) or bilateral (2) areas of distinct hypometabolism that were interpreted as corresponding to epileptogenic foci. Hypometabolism mostly was found in the anterior temporal lobe, including hippocampal structures (9). Moreover, in two cases (P1 and P4), the ipsilateral inferior frontal lobe or, in one case (P7), the inferior part of the anterior insula was affected [12].
SPECT investigations yielded regional abnormalities in five patients.
As well in [Laster OW, Penry JK, Moody OM, 1985]. Compares the efficacy of CT against MRI in 59 patients, which displays MR displayed an abnormal signal in 31 (53%) of the 59 patients. In no instance did MR fail to detect a lesion seen on CT. MR was positive in five patients (16%) in whom CT was negative. 3 of the patients with negative CT and positive MR scans had subtle, poorly defined hyperintense foci in the temporal lobe on T2-weighted images. 2 of the three had aspiration partial lobectomies with relief of seizures. Both MR and the CT were positive in seven patients who had negative EEG findings; 5 of these 7 patients had tumors, one had hemiplegic migraine, and one had focal atrophy after cerebral trauma. In the complex partial seizure subgroup of 34 patients, MR was positive in 15 (44%), CT was positive in 10 (29%), and EEG was positive in 27 (80%).
Twenty-six (44%) of the 59 patients had lobectomies or partial lobectomies. Of these 26, 14 (54%) had neoplasms. Eighteen of the 26 patients who underwent surgery had positive CT and MR scans; 14 of these patients had tumors. The remaining eight patients who had surgery had no CT or MR abnormalities and had temporal lobectomies for intractable seizures; none had tumors. Twenty-eight patients, including eight with positive MR scans, did not undergo surgery. In 19 of the 26 patients who underwent surgery, seizure control was a major goal. Fourteen (74%) of these 19 are now seizure-free, and four (21 %) are greatly improved, with a greater than 75% reduction in the incidence of seizures. One patient was improved but had less than a 75% reduction of seizures.
Table 2. Summary of Abnormalities found in CT, MRI and SPECT. CT MRI SPECT Normal 19 17 11 Lateralising lesion shown 1 7 19 Asymmetry of sylvian fissure or temporal horn shown 10 8 - Bilateral abnormalities shown 0 1 5
Moreover, in [Bronen RA, Fulbright RK, Spencer DD, Spencer SS, Kim JH, Lange RC, Sutilla 1996] the comparison of CT and MRI shows once more time major sensitivity in MRI than CT in patients with refractory epilepsy.
By using these definitions for the 124 surgical and histopathologic findings in the 117 patients, we had sensitivities of 32% (35 of 109) for CT ana 95% (100 for over 109) for MR imaging, positive predictive value of 97% (35 of 36) for CT and 98% (104 of 106) for MR imaging, negative predictive values of 16% (15 of 88) for CT and 72% (13 of 18) for MR imaging, and accuracies of 40% (49 of 124) for CT and 94% (117 of 124) for MR imaging.
The probability that a patient with a negative MR imaging finding would have a positive CT finding was 0%, while the probability that a patient with a negative CT finding would have a positive MR imaging finding was 80%. This analysis in revealed MR imaging sensitivity of 86% (97 of 113) for the identification of the site and 88% (99 of 113) for the prediction of the substrate, while CT sensitivities were 28% (32 of 113) and 35% (40 of 113), respectively. The correct site of survey was identified with MR imaging in 86% of patients (72 of 84) and with CT in 19% of patients (16 of 84) with temporal lobe abnormalities.
Table 3. CT findings in this patient’s group.
Substrate Calcification Contrast Material
Enhancement Temporal Lobe Asymmetry Developmental disorder 1 of 7 (14%) 0 of 7 (0%) O of 7 (0%) Hippocampal sclerosis 0 of 52 (0%) 0 of 47 (0%) 1 of 52 (2%) Tumor 10 of 29 (34%) 7 of 29 (24%) 0 of 29 (0%) Vascular abnormality 4 of 8 (50%) 4 of 8 (50%) 0 of 8 (0%) Indeterminate findings 4 of 28 (14%) 1 of 26 (4%) 4 of 28 (14%) All 19 of 124 (15%) 12 of 110 (11%) 5 of 124 (4%)
Three (3%) of the 117 patients had more than one abnormality detected with CT. MR images in 20 (17%) of the 117 patients showed multiple imaging abnormalities.
Furthermore, [Phuttharak W, Sawanyawisuth K, Kawiwungsanon A, Tiamkao S. 2011], a total of 180 patients with epilepsy underwent into CT and/or MRI investigation; There were 75 PWE who underwent only CT imagines, 85 PWE who underwent only MRI and 20 PWE who underwent both CT and MRI studies. The total numbers of CT and MRI were 95 and 105 data sets which were reviewed. CT scan significantly detected brain abnormalities more than MRI in patients with epilepsy.
Table 4. Abnormal findings in this study
Findings CT (N=95) MRI (N=105) Abnormal 67 (70,5%) 55 (52,4%) Tumor 4 (5,9%) 7 (11,8%) Vascular 4 (5,9%) 4 (6,8) Stroke 25 (37,3%) 7 (11,8%) Trauma 6 (8,9%) 1 (1,7%) Brain atrophy 17 (25,4%) 14 (23,7%) Cysticercosis 9 (13,4%) 1 (1,7%) Congenital 1 (1,5%) 2 (3,4%) Post-brain operation 1 (1,5%) 1 (1,7%) Hippocampal sclerosis 0 (0%) 18 (29,5%)
It was also found that PWE caused by stroke and cysticercosis were statistically higher than MRI, whereas MRI was significantly better in the diagnosis of hippocampal sclerosis. In terms of detecting brain tumor, vascular brain disease, trauma, brain atrophy, congenital brain anomaly, and post-brain operation, there was no statistical significance between these two imaging modalities. Out of 20 patients who had been done both CT and MRI studies, only three patients showed different results between CT and MRI studies. All three patients had normal CT findings but MRI detected herpes encephalitis in two patients and brain atrophy in one patient.
In summary, all the abnormal findings discovered in the reviewed articles are shown in the next chart divided by the imaging technique used.
Graph 1. Comparation of abnormal findings observed in all studies reviewed divided by radiological investigation. 40% 30% 29% 37% 30% 70% 80% 44% 50% 89% 52% 80% 80% 50% 63% 100% 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Guberman Stefan Laster Duncan Bronen Phuttharak
DISCUSSION
The most CT lesions have been found in partial seizures, especially elementary seizures (Angeleri et al., 1980; Bauer et al., 1980; Ghazy et al., 1978; Janz, 1978; Yang et al., 1979), as well as the Lennox-Gastaut and West syndromes (Gastaut et al., 1976; Gastaut et al., 1978; Zimmerman et al., 1977).
Data from other research confirmed our observation that partial seizures with secondary generalization are far more likely to be associated with CT anomalies than purely partial seizures (McGahan et al., 1979), despite the fact that others observed an equal occurrence (Scolo-Lavizzari and Balmer, 1980).
Is remarkable because of the vast number of tumors discovered, the comparatively large number of patients who have undergone lobectomies for seizure therapy, and, ultimately, the high proportion of surgical remedies of epilepsy [13].
Patients with advanced abnormalities, such as cancers, which are more likely to turn up on a CT scan if their epilepsy has been present for a long time, are often more likely to exhibit other neurological signs or symptoms. Others also discovered that late-onset (after the age of 20 or 30) epilepsy has a much higher rate of CT abnormality than early-onset epilepsy (Janz, 1978; Pritchard and Hungerford, 1979).
The true benefit of CT scanning in epilepsy is its ability to diagnose real unexpected lesions unique to the patient's epilepsy. The tumor was unexpected in 3% of 500 cases (Gastaut's 1976), as well as in both of our cases, though there were no signs other than seizures and the neurological test was usual.
Patients with epilepsy affected by cysticercosis was shown to be statistically higher in CT scans than in MRIs. This can be explained by the fact that the majority of cysticercosis patients in that study were in the calcified stage.
With the exception of small areas of calcification, which are better shown by CT, MRI is more sensitive in showing subtle lesions of temporal lobe structures. CT was slightly more effective at detecting anatomical asymmetry [14].
SPECT should be included in the routine workup for temporal lobectomy, according to studies. Although EEG will most likely continue to be the primary lateralizing investigation in most patients, the use of therapies such as MRI and SPECT will not only increase the number of patients eligible for surgery, but can also maximize results in terms of the percentage of patients who recover from improving patient quality.
very good (84-86 percent) for localizing extratemporal and temporal lobe anomalies, CT results were significantly worse, especially for temporal lobe lesions. The ability of MR and CT to distinguish between substrates was found to be significantly different in the same sample. Because of the lack of beam hardening artifact from the skull base, MRI is generally preferable to CT scan for detecting minor brain stem lesions, cerebellar lesions, inferior frontal and temporal lobe lesions. This means that epileptic patients with complex partial seizures or clinical characteristics of encephalitis with hemorrhagic cerebrospinal fluid should have an MRI.
T2-weighted images of the temporal lobe prove to be capable of detecting pathological foci that are not apparent on improved CT scans of the brain. Since partial aspiration lobectomies, both of the patients in who had positive MR and negative CT outcomes became seizure-free.
Despite the fact that other experiments have revealed intrinsic neoplasms on MR that were not discovered on CT. In no case did magnetic resonance imaging (MR) skip a lesion that was apparent on CT.
We recommend that CT examination would be avoided in the diagnostics of patients with recurring seizures in medically refractory epilepsy, even in exceptional cases, such as in patients who are unable to undergo MRI. It appears to be imprudent to use less costly CT imaging instead of MRI.
Interictal experiments of temporal lobe epilepsy using both PET and SPECT have identified focal temporal hypoperfusion as the most frequent abnormality [23-24].
Furthermore, all of the findings confirm the notion that MRI has a significant diagnostic advantage over CT, as stated by Janz et al. 1985.
CONCLUSION
The advantages of MRI over CT scan are numerous and do not need further elaboration. However, the disadvantages of MRI are its unavailability for larger number of patients, higher cost, and the requirement for longer time periods for scanning.
REFERENCES
1. Oseph I. Sirven MDPatty Obsorne Shafer RN, MNon. What is Epilepsy? January 21, 2014.
2. National Institute of Neurological Disorders and Stroke. The epilepsies and seizures: hope through. 8/10/2015.
3. Schachter, S. C., Shafer, P. O, & Sirven, J. I. (2013, August). Triggers of seizures. 4. Sá de Camargo EC, Koroshetz WJ. Neuroimaging of ischemia and infarction. NeuroRx.
2005 Apr;2(2):265-76. doi: 10.1602/neurorx.2.2.265. PMID: 15897950; PMCID: PMC1064991.
5. Ives JR, Gloor P. New sphenoidal electrode assembly to permit long-term monitoring of the patient's ictal or interictal EEG. Electroencephalogr Clin Neurophysiol. 1977 Apr;42(4):575-80. doi: 10.1016/0013-4694(77)90221-8. PMID: 66141.
6. Wienhard K, Pawlik G, Herholz K, Wagner R, Heiss WD. Estimation of local cerebral glucose utilization by positron emission tomography of [18F]2-fluoro-2-deoxy-D-glucose: a critical appraisal of optimization procedures. J Cereb Blood Flow Metab. 1985 Mar;5(1):115-25. doi: 10.1038/jcbfm.1985.15. PMID: 3871780.
7. L. Eriksson et al., "A Four Ring Positron Camera System for Emission Tomography of the Brain," in IEEE Transactions on Nuclear Science, vol. 29, no. 1, pp. 539-543, Feb. 1982, doi: 10.1109/TNS.1982.4335903.
8. Herholz K, Pawlik G, Wienhard K, Heiss WD. Computer assisted mapping in quantitative analysis of cerebral positron emission tomograms. J Comput Assist Tomogr. 1985 Jan-Feb;9(1):154-61. doi: 10.1097/00004728-198501000-00026. PMID: 3871445.
9. Devous MD Sr. Single-photon emission computed tomography in neurotherapeutics. NeuroRx. 2005 Apr;2(2):237-49. doi: 10.1602/neurorx.2.2.237. PMID: 15897948; PMCID: PMC1064989.
10. Horsley V. An Address on the Origin and Seat of Epileptic Disturbance: Delivered before the Cardiff Medical Society. Br Med J. 1892 Apr 2;1(1631):693-6. doi: 10.1136/bmj.1.1631.693. PMID: 20753617; PMCID: PMC2420022.
Symposium 1986: Radioaktive Isotope in Klinik und Forschung. Egermann, Wien, pp 33-38.
12. Kuhl DE, Engel J Jr, Phelps ME, Selin C (1980) Epileptic pat- terns of local cerebral metabolism and perfusion in humans deter- mined by emission computed tomography of 18FDG and 13NH3. Ann Neurol 8:348-360
13. Laster OW, Penry JK, Moody OM, et al. Chronic seizure disorders: contribution of MR imaging when CT is normal. AJNR 1985;6:177-180
14. Stefan, H., Pawlik, G., Böcher-Schwarz, H.G. et al. Functional and morphological abnormalities in temporal lobe epilepsy: a comparison of interictal and ictal EEG, CT, MRI, SPECT and PET. J Neurol 234, 377–384 (1987). doi:10.1007/BF00314081
15. Bronen RA, Fulbright RK, Spencer DD, Spencer SS, Kim JH, Lange RC, Sutilla C. Refractory epilepsy: comparison of MR imaging, CT, and histopathologic findings in 117 patients. Radiology. 1996 Oct;201(1):97-105. doi:
10.1148/radiology.201.1.8816528. PMID: 8816528
16. Phuttharak W, Sawanyawisuth K, Kawiwungsanon A, Tiamkao S. The appropriate neuroimaging study in persons with epilepsy. Neurol Sci. 2011 Oct;32(5):969-71. doi: 10.1007/s10072-011-0640-2. Epub 2011 Jun 7. PMID: 21647630.
17. Guberman, A. (1983). The Role of Computed Cranial Tomography (CT) in Epilepsy. Canadian Journal of Neurological Sciences / Journal Canadien Des Sciences
Neurologiques, 10(1), 16-21. doi:10.1017/S0317167100044504.
18. Schorner W, Meenke HJ, Felix R.Temporal lobe epilepsy: comparison of CT and MR imaging. Am J Neuroradiol 1987;8:773-81.
19. Lesser RF, Modic MT, Weinstein MA, et al. Magnetic resonanceimaging(1-5Tesla)in patients with intractable focal seizures. ArchNeurol1986;43:367-71.
20. Sperling MR, Wilson G, Engel J, Babb TL, Phelps M, Bradley M. Magnetic resonance imaging in intractable partial epilepsy: correlative studies. Ann Neurol 1986;20:57-62.
21. Theodore WH, Dorwart R, Holmes M, Porter RJ, DiChiro G. Neuroimaging in
refractory partial seizures. Comparison of PET, CT and MRI. Neurology1986;36:750-9. 22. Triulzi F, Francheschi M, Fazzio F, Del Maschio A. Nonrefractory temporal lobe
epilepsy: 1-5T MR imaging. Radiology 1988;166:181-5.
24. Hougaard K, Oikawa T, Sveinsodittir E, Skinhoj E, Ingvar DH, Lassen NA. Regional cerebral blood flow in focal cortical epilepsy. Arch Neurol 1976;33:527-35.
25. Engel J. The use of positron emission tomographic scanning in epilepsy. Ann Neurol 1984;15:S180-191.
26. Janz D, Meenke HJ, Sch6rner W (1985) Kernspintomographische Untersuchungen (MRT) bei Patienten mit Temporallappen-Epi- lepsie. In: Kruse R (ed) Epilepsie 84. Einhorn, Reinbek, pp 238- 242
