doi:10.1684/epd.2013.0572
pressure [CPP]) depends on two parameters: the a discrete tonic flexion of his superior limbs. During median arterial pressure (MAP) and the intracranial some of the episodes, he yawned, snored, perspired pressure (ICP), which is the pressure inside the skull profusely, and had bilateral mydriasis and facial red- and thus in the brain tissue and cerebrospinal fluid ness. These episodes would last several minutes and (CSF). afterwards the patient would recover consciousness Many disorders can cause syncope. The most common with short or non-existent postictal confusion. These are classified as neurally-mediated syncope (vaso- events would occur at any time of the day, whether vagal syncope), cardiac arrhythmias, and orthostatic sitting or standing, and the patient did not identify any hypotension (Brignole et al., 2004; Miller and Kruse, triggers. At first, the episodes could be aborted at onset 2005). Uncommon aetiologies, such as metabolic or by lying down, but later they became unresponsive to neurological disorders, should be considered when postural change (see video sequence). other causes have been ruled out (Jhanjee et al., 2006), The patient’s neurological and physical examinations including episodes of transient increase of intracranial were normal except for a chronic bilateral papil- pressure. loedema which was not resolved, despite the shunt. We present a case of a patient with recurrent loss of The results of various blood tests, cerebral MRI, interic- consciousness of unknown aetiology in which video- tal EEG, electrocardiography (ECG), echocardiography, electroencephalogram (VEEG) monitoring indicated a and Holter-electrocardiography did not reveal any diagnosis of syncope with uncommon aetiology. anomaly. During the tilt-test, and with the adminis- tration of nitro-glycerine, the patient experienced a loss of consciousness but reported that “this time it Case report was different because I did not experience the usual symptoms”. A 37-year-old, right-handed man was referred to the Different possible aetiologies were considered. Cere- Epilepsy Unit for the evaluation of episodes of uncon- bral MRI venography (MRV) revealed a chronic partial sciousness that had begun two months earlier. He was superior longitudinal sinus thrombosis, and several born after an uneventful pregnancy, at term, to non- EEGs did not show epileptiform activity. Nevertheless, consanguineous parents, and his development was epilepsy was considered probable and thus antiepilep- normal. There was no family history of epilepsy. He tic treatment was introduced (levetiracetam, up to had suffered two episodes of venous thrombosis at the 2000 mg a day). The patient experienced a reduction ages of 20 and 22, respectively. In the first episode, he in the number of episodes, which did not completely experienced discomfort, dyspnoea, and facial redness; disappear. VEEG monitoring recorded several events, he was diagnosed with superior vena cava thrombosis identified by the family and the patient as “his usual and was prescribed anticoagulants for six months. Two epileptic seizures”. Arterial blood pressure, heart rate, years later, he started to have headaches, diplopia, and and glycaemia were normal during the episodes. The paresis of the sixth cranial nerve. Cerebral MRI showed patient recovered without confusion from each event, a superior longitudinal sinus cerebral thrombosis and although he did not remember the episode. Simul- therefore anticoagulant treatment was reintroduced. taneous EEG showed a generalised, theta activity, Testing apparently revealed protein C and S deficiency followed by hypersynchronous, diffused, delta activity and anticoagulant therapy was therefore continued of high voltage with frontal predominance. When the indefinitely. During the following year, he remained patient recovered, this activity disappeared following a asymptomatic, however, during a routine consulta- reverse sequence (each episode lasted for 5-8 minutes) tion, a bilateral papilloedema was discovered and a (figure 1). In some of the episodes, a slow-flat-slow lumbar puncture demonstrated high intracranial pres- pattern was observed. The interictal EEG showed sure. Due to these findings, a lumboperitoneal shunt general and discrete slowing-down without any was inserted and during the subsequent 14 years, the epileptiform abnormalities. patient did not experience any medical problems. These EEG alterations are similar to the pattern At the age of 36, the patient presented with paroxys- observed during syncope but neither blood pressure tic, transient episodes of loss of consciousness. On nor heart rate changed, therefore cardiac arrhyth- presentation, these events were sporadic but they mias, vasovagal episodes and orthostatic hypotension increased in severity and frequency, such that by the were ruled out. This led us to consider other less time he came to our attention, the episodes were frequent causes of cerebral hypoperfusion, such as occurring almost daily. During these episodes, he typi- an increase in ICP. We performed a lumbar puncture cally experienced malaise and dizziness, accompanied which demonstrated an ICP of 47 mm Hg. Lum- by generalised weakness. After several seconds, he lost bar cisternography revealed that the lumboperitoneal consciousness but his eyes would remain open and the shunt was not working properly. Cerebral arterio- family reported that he stayed motionless, except for graphy showed partial and chronic thrombosis of all
176 Epileptic Disord, Vol. 15, No. 2, June 2013 Venous cerebral thrombosis and syncope
A
*Fp1-F3 F3-C3 C3-P3 P3-O1
*Fp2-F4 F4-C4 C4-P4 P4-O2
*Fp1-F7 F7-T3 T3-T5 T5-O1
*Fp2-F8 F8-T4 T4-T6 T6-O2
Fz-Cz Cz-Pz T1-T2
*EKG1-EKG2
B
Fp1-F3
F3-C3
C3-P3
P3-O1
Fp2-F4 F4-C4 C4-P4 P4-O2
Fp1-F7
F7-T3
T3-T5
T5-O1
Fp2-F8 F8-T4 T4-T6 T6-O2
Fz-Cz Cz-Pz T1-T2
*EKG1-EKG2
Figure 1. EEG recording in an average montage during an epileptic seizure. (A) EEG showing the generalised theta activity at the beginning of the episode. (B and C) After a few seconds, this activity was followed by hypersynchronous, diffused, delta activity of high voltage with frontal predominance. (D) When the patient recovered, the activity disappeared and the EEG normalised, following a reverse sequence. There were no alterations on the ECG.
Epileptic Disord, Vol. 15, No. 2, June 2013 177 M.E.G. García, et al.
C
Fp1-F3
F3-C3
C3-P3
P3-O1
Fp2-F4 F4-C4 C4-P4 P4-O2
Fp1-F7
F7-T3
T3-T5
T5-O1
Fp2-F8 F8-T4 T4-T6 T6-O2
Fz-Cz Cz-Pz T1-T2
*EKG1-EKG2
D
Fp1-F3
F3-C3
C3-P3
P3-O1
Fp2-F4 F4-C4 C4-P4 P4-O2
Fp1-F7
F7-T3
T3-T5
T5-O1
Fp2-F8 F8-T4 T4-T6 T6-O2
Fz-Cz Cz-Pz T1-T2
*EKG1-EKG2
Figure 1. (Continued) the cerebral sinuses and of both of the internal jugular endovascular treatment was rejected. The lumbo- veins. Venous return occurred through the vertebral peritoneal shunt was replaced and since then, plexus and external facial veins (figure 2). The superior the patient has been free of episodes. A 24-hour cava vein, the brachiocephalic trunk, and the sub- period of VEEG monitoring performed one month clavian vein were also thrombosed, as seen on chest later was completely normal. Antiepileptic treat- computed tomography. ment was slowly withdrawn. A new coagulation Because the thrombosis was chronic (as demon- test did not show protein C and S deficiency, but strated by significant collateral circulation), fibrinolytic instead high levels of anticardiolipin antibodies were
178 Epileptic Disord, Vol. 15, No. 2, June 2013 Venous cerebral thrombosis and syncope
these events in which we identified an EEG pattern typically described during syncope. This pattern is characterised by the early appearance of slow, high- voltage activity in the theta range, followed by a further slowing-down in the delta range, and is considered to be similar for all types of syncope, regardless of aetiology (Brenner, 1997; Mecarelli et al., 2004). If the hypoperfusion continues, the electrocerebral activity disappears and a flat EEG recording appears (convulsive syncope may occur at this time). After the syncope, the EEG activity normalises, following a reverse sequence (Ammirati et al., 1998). In our case, the pattern observed during these episodes showed generalised, diffuse, theta activity, followed by increased amplitude and reduced-frequency, brain-wave activity (delta activity.) There was also a flattening of the electrocerebral activity (during 2-4 seconds) in the middle of this delta activity. This flattening may indicate a further cerebral hypoperfusion and is more commonly associated with cardioinhibitory syncope than vasovagal syncope. What is surprising in our case is the longer duration of the episodes compared with what is reported in the literature (less than a minute). This might be because the majority of syncopes with EEG correlates described in the literature are cardioinhibitory syncopes or vasodepressor syncopes, and the aetiology in our case was different. Figure 2. Cerebral arteriography: chronic and partial thrombo- We hypothesized that our patient was suffering sis of all cerebral sinuses with significant collateral circulation from episodes of significant and sharp increases through the vertebral plexus, external facial vein, and diploic veins. in ICP due to further cerebral sinus thrombosis and/or lumboperitoneal shunt failure (plateau-waves). Plateau-waves peak during several minutes before repeatedly found. Upon further questioning, the decreasing spontaneously and in each episode, a patient revealed a history of recurrent episodes of decrease of cerebral blood flow leads to global cere- arthritis, mouth and genital ulcers, and thrombo- bral ischaemia, hypoperfusion, and syncope (Hayashi phlebitis. Taking into account the results of the et al., 1991; Chazal et al., 1984; Jedynak et al., 1984). clinical tests, and in the context of the new clinical data, The EEG pattern observed during the plateau phase Bec¸het disease was suspected and immunosuppres- is similar to that during syncope (Naquet and Bostem, sive therapy was initiated in addition to anticoagulants. 1964). The results of the cerebral arteriography and cis- ternography confirmed our hypothesis regarding the Discussion increase in ICP. The initial normal MRI can be explained by the fact We present the case of a young male patient with a that the appearance of the thrombus on MRI within background of two episodes of thrombosis (a cerebral the dural sinus or cortical veins is variable and largely venous thrombosis and a vena cava thrombosis) who dependent on its age. The diagnosis of the later presented with frequent, repetitive, transient episodes stages of cerebral sinus thrombosis (chronic or par- of loss of consciousness. tially recanalized) may be confirmed by MRI in some Obtaining information about a paroxysmal event in cases, but often there is neither a clear thrombus which a patient is unconscious represents a challenge. signal nor clear absence of blood flow (Filippidis et al., Furthermore, the patient is often asymptomatic upon 2009; Isensee et al., 1994). examination and test results can be normal. Epilep- Although the patient had been taking anticoagulants tic seizures and syncope are the two aetiologies most appropriately for many years, this treatment had not often considered (Britton and Benarroch, 2006). been sufficient to prevent further cerebral venous In our case, VEEG monitoring with simultaneous thrombosis. High levels of anticardiolipin antibodies ECG allowed us to record and analyse several of and the patient’s history pointed towards Bec¸het syn-
Epileptic Disord, Vol. 15, No. 2, June 2013 179 M.E.G. García, et al.
drome. Although we cannot conclude that our patient References had Bec¸het disease (the major criteria and one of the minor criteria were met), this was highly likely given Ammirati F, Colivicchi F, Di Battista G, et al. Electroencephalo- the large number of commonly associated symptoms graphic correlates of vasovagal syncope induced by head-up presented (including dural sinus thrombosis) (Erdem tilt testing. Stroke 1998; 29: 2347-51. et al., 2006). Brenner RP. Electroencephalography in syncope. J Clin Neu- rophysiol 1997; 14: 197-209.
Conclusion Brignole M, Alboni P, Benditt D, et al. Guidelines on manage- ment (diagnosis and treatment) of syncope. Update 2004. Eur Two issues are of particular interest in this case. Heart J 2004; 25: 2054-72. Firstly, the usefulness of performing VEEG monitoring Britton JW, Benarroch E. Seizures and syncope: anatomic with simultaneous ECG in all patients who experience basis and diagnostic considerations. Clin Auton Res episodes of loss of consciousness of unknown cause, 2006; 16: 18-28. and secondly, the need to study all possible causes of cerebral hypoperfusion in a patient with repeat Chazal J, Janny P, Irthum B, et al. Plateau wave, unexpected syncope. cause of anoxo-ischemic syncope. Reflections on the patho- genesis of the plateau wave apropos of a case. Neurochirurgie 1984; 30: 277-81. Acknowledgements and disclosures. We would like to thank Professor John Stephenson (Glasgow) for Erdem H, Dinc¸A, Pay S, et al. A neuro-Behc¸et’s case compli- his constructive contribution to the article and also Alex Thee- cated with intracranial hypertension successfully treated by dom for his assistance in preparation. This work has not been a lumboperitoneal shunt. Joint Bone Spine 2006; 73: 200-1. supported by any grant and has not been presented or published in any form. Filippidis A, Kapsalaki E, Patramani G, et al. Cerebral venous None of the authors has any conflict of interests to disclose. sinus thrombosis: review of the demographics, pathophys- iology, current diagnosis, and treatment. Neurosurg Focus Legends for video sequences 2009; 27: E3. Hayashi M, Handa Y, Kobayashi H, et al. Plateau-wave phe- Video sequence 1 nomenon (I). Correlation between the appearance of plateau waves and CSF circulation in patients with intracranial hyper- The video shows a typical seizure of the patient. The tension. Brain 1991; 114: 2681-91. event starts when the patient feels faint, warns the Isensee C, Reul J, Thron A. Magnetic resonance imaging of family,and lies down. He then losses consciousness, thrombosed dural sinuses. Stroke 1994; 25: 29-34. remains still, apart from occasional movements of his left hand and leg, and yawns occasionally. The Jedynak CP, Fournier L, Fischler M, et al. Loss of conscious- episode lasts for seven minutes after which he ness during benign intracranial hypertension. Correlations recovers with no postictal period. between cerebrospinal fluid pressure and the electroen- The EEG shows a generalised theta activity, followed cephalogram. Rev Neurol (Paris) 1984; 140: 217-20. by hypersynchronous diffused delta activity of high voltage with frontal predominance. A slow-flat-slow Jhanjee R, Van Dijk JG, Sakaguchi S, et al. Syncope in adults: pattern is also observed. This activity disappears terminology, classification and diagnostic strategy. Pacing Clin Electrophysiol 2006; 29: 1160-9. following a reverse sequence when the patient recovers. Kapoor WN. Syncope. N Engl J Med 2000; 343: 1856-62.
Key words for video research on Mecarelli O, Pulitan P, Vicenzini E, et al. Observations on www.epilepticdisorders.com EEG patterns in neurally-mediated syncope: an inspective and Syndrome: non epileptic paroxysmal disorder quantitative study. Neurophysiol Clin 2004; 34: 203-7. Etiology: venous thrombosis Phenomenology: Miller T, Kruse J. Evaluation of syncope. Am Fam Physician dizziness; 2005; 72: 1492-500. nonepileptic paroxysmal event; consciousness (loss) Naquet R, Bostem F. Electhoencephalographic study of Localization: not applicable syncope. Electroencephalogr Clin Neurophysiol 1964; 16: 140-52.
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