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Paroxysmal bipedal activity during syncope related to carotid body tumor
Epilepsy & Behavior 15 (2009) 388–390
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Case Report
Paroxysmal bipedal activity during syncope related to carotid body tumor Giovanni Ambrosetto, Pasquale Montagna, Roberto Vetrugno *, Pietro Cortelli Department of Neurological Sciences, University of Bologna, Bologna, Italy
a r t i c l e
i n f o
Article history: Received 18 March 2009 Revised 1 April 2009 Accepted 4 April 2009 Available online 6 May 2009 Keywords: Syncope Paroxysmal bipedal activity Carotid body tumor Central pattern generators Frontal lobe epilepsy Neuroethology
a b s t r a c t Involuntary patterned motor activity may occur during seizures, especially those of frontal lobe origin, and during transient ischemic attacks. Paroxysmal patterned motor activity in frontal lobe epilepsy has been attributed to direct involvement of mesial frontal regions by the epileptic discharge. Paroxysmal bipedal frenetic activity occurred during an episode of syncope in a patient with a carotid body tumor. The presence of rhythmic motor patterns similar to the epileptic ones also during syncope and cerebral ischemia suggest a phenomenon of release from neocortical inactivation, probably of innate motor behaviors generated by neural networks referred to as central pattern generators (CPGs). Ó 2009 Elsevier Inc. All rights reserved.
1. Introduction Paroxysmal bipedal activity (PBA) is an automatism of frenetic, alternating flexion and extension of the lower limbs. It usually occurs in association with intensively affective vocal and facial expression and bimanual and axial activity in sleep-related seizures of mesial frontal lobe origin [1]. The term hypermotor (hyperkinetic) seizures was coined to describe such epileptic seizures [2]. At times, transient cerebral ischemic attacks may mimic epileptic generalized tonic or tonic–clonic seizures as well as simple partial motor seizures. We report a case of PBA occurring during episodes of syncope related to a carotid body tumor. 2. Report of a case A 35-year-old woman was admitted with a 3-year history of transient episodes of loss of consciousness. She reported longstanding lightheadedness, cold sweating, and sudden temporomandibular pain prior to loss of consciousness. Spells lasted less than 1 min and were followed by immediate and complete recovery. The frequency of episodes was one a month at the beginning, progressively increasing to two or three a week at the time of our observation. Several spells occurred during nocturnal sleep, when she was awoken by temporomandibular pain followed by loss of consciousness and uncoordinated limb movements. * Corresponding author. Address: Dipartimento di Scienze Neurologiche dell’Università di Bologna, Via Ugo Foscolo 7, 40123 Bologna, Italy. Fax: +39 051 2092963. E-mail address: [email protected] (R. Vetrugno). 1525-5050/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2009.04.003
Neurological and psychological examination, routine laboratory tests, resting and stress ECG, EEG, tilt-up test, and heart and brain MRI were all normal. Vitaport recording showed heart arrhythmia and captured a prolonged ECG pause resolving with an awakening from REM sleep (Fig. 1) During a second nocturnal video-polysomnography, at morning awakening, the patient had a syncopal episode characterized by the usual prodromic sensation of temporomandibular pain and facial paling and sweating associated with vasodepression, followed by cardioinhibition and syncope. Video-polygraphic findings showed behavioral unresponsiveness, immediately followed by loss of consciousness with ECG asystolia, accompanied by bipedal motor activity and generalized stiffness, and followed by spontaneous recovery 10 s after the beginning of the attack (Fig. 2). Doppler of the carotids and neck CT revealed a highly vascularized tumor with splaying of the left internal and external carotids. The patient underwent surgery to remove the tumor, after which she was free of syncope (3 years to date). Subsequent autonomic tests proved normal. Transthoracic ECGs, obtained before and following removal of the carotid body tumor, were normal. 3. Discussion Rhythmic, nonjerking, motor manifestations are extremely rare in syncope. An extensive videometric study of episodes of generalized cerebral hypoxia revealed no movements of this kind [3], but we believe that lower limb automatisms in syncope have not been previously reported as sleep-related syncope is rare. Moreover, syncope during sleep is poorly described because, for a correct diagnosis, polysomnographic recordings are required, which are
G. Ambrosetto et al. / Epilepsy & Behavior 15 (2009) 388–390
389
Fig. 1. Polysomnographic recording showing a sinus arrest during a spontaneous awakening from REM sleep. Systemic arterial pressure and heart rate start to wane before the cardiac pause (systemic arterial pressure reaching the lowest values during the protracted asystolia), waxing again during the ‘‘backing to life.” The EEG (first two channels) shows artifacts and no epileptiform discharge. EOG, electro-oculogram; Mylo., electromyogram of the mylohyoideus; System. Art. Press., systemic arterial pressure; T-A resp., thoracic–abdominal respirogram.
Fig. 2. Video-polygraphic recording showing an episode of loss of consciousness followed by paroxysmal bipedal activity (PBA) and generalized tonic stiffening. The EEG shows slowing and muscle artifacts. Note the ongoing, until undetectable, lowering of systemic arterial pressure values. Five minutes before the episode, blood pressure and heart rate values were within normal range. EOG, electro-oculogram; Mylo., electromyogram of the mylohioideus; T-A resp., thoracic–abdominal respirogram; System. Art. Press., systemic arterial pressure.
not routinely performed. Rhythmic mandibular movements superposable on epileptic masticatory automatisms were reported in a patient with multiple system atrophy and postural hypotension
[4]. Rhythmic bipedal activity in syncope might represent a motor pattern superimposable on sleep-related epileptic bipedal automatisms.
390
G. Ambrosetto et al. / Epilepsy & Behavior 15 (2009) 388–390
Arousal during sleep is reported to induce rhythmic motor patterns of different origin, synchronous or alternating on both sides of the body [5]. Sleep bruxism has been related to microarousals [6]. Meletti et al. reported a case of ictal bruxism induced by temporal lobe seizures [7]. Rhythmic alternating leg muscle activation occurred particularly during arousals in 16 patients polysomnographically recorded for sleep disturbances [8]. Ictal bipedal activity is found in sleep-related epileptic seizures of frontal lobe origin, which are facilitated by the arousal or, alternatively, induce the arousal. In our patient, the clinical features of PBA were similar to those usually observed in hypermotor seizures, only the paroxysmal stepping was faster. PBA in syncope during sleep may represent a similar rhythmic motor pattern related to a phenomenon of release from neocortical inactivation by anoxia. We also conceive of arousal as the unifying factor in PBA related to both ictal cortical discharge and cortical anoxia. In our patient, PBA occurred at the end of ECG asystolia and persisted, along with the final stiffening, at the resumption of heart activity. We speculate that efficacious blood perfusion of spinal cord and brainstem preceded that of cerebral cortex, producing a cortical–subcortical disconnection phenomenon, with complete loss of consciousness and persistence of motor activity. Physiological rhythmic movements, synchronous or alternating on both sides of the body, are innate motor behaviors generated by neural networks referred to as central pattern generators (CPGs), which contain the information for intersegmental coordination necessary for rhythmic motor patterns [9]. Location of CPGs is related to the motor behavior, being in the brainstem for chewing and respiration and in the spinal cord for walking, swimming, and hopping [10,11]. PBA in our patient closely resembled infant stepping, a prelocomotion alternating motor pattern, probably related to the activation of a spinal CPG generating independent walking [12]. We suggest that release of that CPG via anoxic cortical inactivation underlies the pathophysiology of bipedal activity related to the syncope in our case. Furthermore, epileptic bipedal activity might have a similar origin, with cortical inactivation related to the ictal discharge or ictal ignition of a cortical/subcortical CPG by way of corticofugal pathways. Nonparoxysmal stereotyped stepping has been reported in a stuporous man with meningoencephalitis and bilateral necrotic lesions in the medial frontoparietal cortices [13], a cortical zone that is an origin of epileptic seizures with PBA. Recurrent syncope as a complication or the presenting feature of neck malignancy, carotid body tumor included, is an uncommon but well-documented association [14]. The accepted mechanism implies abnormal afferent discharges from the carotid body causing excessive vagal activity. We excluded the diagnosis of frontal lobe epileptic seizures in our patient because of the initial lipothymic signs, subsequent complete loss of consciousness, and late symmetrical stiffening. Nocturnal frontal lobe epileptic seizures usually manifest with impairment of consciousness, no pallor and sweating, and asymmetrical dystonic posturing [1]. Moreover, no EEG epileptic activity was observed during the episode, and attacks completely subsided after removal of the carotid body tumor.
We suggest that different etiologies may underlie superimposable motor patterns with the mechanism of cortical/subcortical disconnection in conditions of altered vigilance. Extensive semiological and polygraphic studies of bipedal activity of various origins may contribute to clarification of this aspect. Ethical approval We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. A signed consent form authorizing publication has been obtained for the patient identified in the photographs accompanying this article. Conflict of interest None of the authors has any conflict of interest to disclose. Acknowledgment We are grateful to Ms. Alessandra Laffi for editing and secretarial assistance in preparing the article. References [1] Wada JA. Predominantly nocturnal recurrence of intensively affective vocal and facial expression associated with powerful bimanual, bipedal and axial activity as ictal manifestations of mesial frontal lobe epilepsy. Adv Epileptol 1989;17:261–7. [2] Lüders H, Acharya J, Baumgartner C, et al. Semiological seizure classification. Epilepsia 1998;39:1006–13. [3] Lempert T, Bauer M, Schmidt D. Syncope: a videometric analysis of 56 episodes of transient hypoxia. Ann Neurol 1994;36:233–7. [4] Iani C, Attanasio A, Manfredi M. Paroxysmal staring and masticatory automatisms during postural hypotension in a patient with multiple system atrophy. Epilepsia 1996;37:690–3. [5] Tassinari CA, Rubboli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias: a neuroethologic approach. Neurol Sci 2005;26(Suppl. 3):s225–32. [6] Macaluso GM, Guerra P, Di Giovanni G, Boselli M, Parrino L, Terzano GM. Sleep bruxism is a disorder related to periodic arousals during sleep. J Dent Res 1998;77:565–73. [7] Meletti S, Cantalupo G, Volpi L, Rubboli G, Magaudda A, Tassinari CA. Rhythmic teeth grinding induced by temporal lobe seizures. Neurology 2004;62:2306–9. [8] Chervin RD, Consens FB, Kutluay E. Alternating leg muscle activation during sleep and arousals: a new sleep-related motor phenomenon? Mov Disord 2003;35:551–9. [9] Grillner S. The motor infrastructure: from ion channels to neural networks. Nat Rev Neurosci 2003;4:573–86. [10] Nakamura Y, Katakura N. Generation of masticatory rhythm in the brainstem. Neurosci Res 1995;23:1–19. [11] Kiehn O, Kjaerulff O. Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 1998;16:110–29. [12] Yang JF, Lam T, Pang MY, Lamont E, Musselman K, Seinen E. Infant stepping: a window to the behaviour of the human pattern generator for walking. Can J Physiol Pharmacol 2004;82:662–74. [13] Sato S, Hashimoto T, Nakamura A, Ikeda S. Stereotyped stepping associated with lesions in the bilateral medial frontotemporal cortices. Neurology 2001;57:711–3. [14] Worth PF, Stevens JC, Lasri F, et al. Syncope associated with pain as the presenting feature of neck malignancy: failure of cardiac pacemaker to prevent attacks in two cases. J Neurol Neurosurg Psychiatry 2005;76:1301–3.
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Case Report
Paroxysmal bipedal activity during syncope related to carotid body tumor Giovanni Ambrosetto, Pasquale Montagna, Roberto Vetrugno *, Pietro Cortelli Department of Neurological Sciences, University of Bologna, Bologna, Italy
a r t i c l e
i n f o
Article history: Received 18 March 2009 Revised 1 April 2009 Accepted 4 April 2009 Available online 6 May 2009 Keywords: Syncope Paroxysmal bipedal activity Carotid body tumor Central pattern generators Frontal lobe epilepsy Neuroethology
a b s t r a c t Involuntary patterned motor activity may occur during seizures, especially those of frontal lobe origin, and during transient ischemic attacks. Paroxysmal patterned motor activity in frontal lobe epilepsy has been attributed to direct involvement of mesial frontal regions by the epileptic discharge. Paroxysmal bipedal frenetic activity occurred during an episode of syncope in a patient with a carotid body tumor. The presence of rhythmic motor patterns similar to the epileptic ones also during syncope and cerebral ischemia suggest a phenomenon of release from neocortical inactivation, probably of innate motor behaviors generated by neural networks referred to as central pattern generators (CPGs). Ó 2009 Elsevier Inc. All rights reserved.
1. Introduction Paroxysmal bipedal activity (PBA) is an automatism of frenetic, alternating flexion and extension of the lower limbs. It usually occurs in association with intensively affective vocal and facial expression and bimanual and axial activity in sleep-related seizures of mesial frontal lobe origin [1]. The term hypermotor (hyperkinetic) seizures was coined to describe such epileptic seizures [2]. At times, transient cerebral ischemic attacks may mimic epileptic generalized tonic or tonic–clonic seizures as well as simple partial motor seizures. We report a case of PBA occurring during episodes of syncope related to a carotid body tumor. 2. Report of a case A 35-year-old woman was admitted with a 3-year history of transient episodes of loss of consciousness. She reported longstanding lightheadedness, cold sweating, and sudden temporomandibular pain prior to loss of consciousness. Spells lasted less than 1 min and were followed by immediate and complete recovery. The frequency of episodes was one a month at the beginning, progressively increasing to two or three a week at the time of our observation. Several spells occurred during nocturnal sleep, when she was awoken by temporomandibular pain followed by loss of consciousness and uncoordinated limb movements. * Corresponding author. Address: Dipartimento di Scienze Neurologiche dell’Università di Bologna, Via Ugo Foscolo 7, 40123 Bologna, Italy. Fax: +39 051 2092963. E-mail address: [email protected] (R. Vetrugno). 1525-5050/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2009.04.003
Neurological and psychological examination, routine laboratory tests, resting and stress ECG, EEG, tilt-up test, and heart and brain MRI were all normal. Vitaport recording showed heart arrhythmia and captured a prolonged ECG pause resolving with an awakening from REM sleep (Fig. 1) During a second nocturnal video-polysomnography, at morning awakening, the patient had a syncopal episode characterized by the usual prodromic sensation of temporomandibular pain and facial paling and sweating associated with vasodepression, followed by cardioinhibition and syncope. Video-polygraphic findings showed behavioral unresponsiveness, immediately followed by loss of consciousness with ECG asystolia, accompanied by bipedal motor activity and generalized stiffness, and followed by spontaneous recovery 10 s after the beginning of the attack (Fig. 2). Doppler of the carotids and neck CT revealed a highly vascularized tumor with splaying of the left internal and external carotids. The patient underwent surgery to remove the tumor, after which she was free of syncope (3 years to date). Subsequent autonomic tests proved normal. Transthoracic ECGs, obtained before and following removal of the carotid body tumor, were normal. 3. Discussion Rhythmic, nonjerking, motor manifestations are extremely rare in syncope. An extensive videometric study of episodes of generalized cerebral hypoxia revealed no movements of this kind [3], but we believe that lower limb automatisms in syncope have not been previously reported as sleep-related syncope is rare. Moreover, syncope during sleep is poorly described because, for a correct diagnosis, polysomnographic recordings are required, which are
G. Ambrosetto et al. / Epilepsy & Behavior 15 (2009) 388–390
389
Fig. 1. Polysomnographic recording showing a sinus arrest during a spontaneous awakening from REM sleep. Systemic arterial pressure and heart rate start to wane before the cardiac pause (systemic arterial pressure reaching the lowest values during the protracted asystolia), waxing again during the ‘‘backing to life.” The EEG (first two channels) shows artifacts and no epileptiform discharge. EOG, electro-oculogram; Mylo., electromyogram of the mylohyoideus; System. Art. Press., systemic arterial pressure; T-A resp., thoracic–abdominal respirogram.
Fig. 2. Video-polygraphic recording showing an episode of loss of consciousness followed by paroxysmal bipedal activity (PBA) and generalized tonic stiffening. The EEG shows slowing and muscle artifacts. Note the ongoing, until undetectable, lowering of systemic arterial pressure values. Five minutes before the episode, blood pressure and heart rate values were within normal range. EOG, electro-oculogram; Mylo., electromyogram of the mylohioideus; T-A resp., thoracic–abdominal respirogram; System. Art. Press., systemic arterial pressure.
not routinely performed. Rhythmic mandibular movements superposable on epileptic masticatory automatisms were reported in a patient with multiple system atrophy and postural hypotension
[4]. Rhythmic bipedal activity in syncope might represent a motor pattern superimposable on sleep-related epileptic bipedal automatisms.
390
G. Ambrosetto et al. / Epilepsy & Behavior 15 (2009) 388–390
Arousal during sleep is reported to induce rhythmic motor patterns of different origin, synchronous or alternating on both sides of the body [5]. Sleep bruxism has been related to microarousals [6]. Meletti et al. reported a case of ictal bruxism induced by temporal lobe seizures [7]. Rhythmic alternating leg muscle activation occurred particularly during arousals in 16 patients polysomnographically recorded for sleep disturbances [8]. Ictal bipedal activity is found in sleep-related epileptic seizures of frontal lobe origin, which are facilitated by the arousal or, alternatively, induce the arousal. In our patient, the clinical features of PBA were similar to those usually observed in hypermotor seizures, only the paroxysmal stepping was faster. PBA in syncope during sleep may represent a similar rhythmic motor pattern related to a phenomenon of release from neocortical inactivation by anoxia. We also conceive of arousal as the unifying factor in PBA related to both ictal cortical discharge and cortical anoxia. In our patient, PBA occurred at the end of ECG asystolia and persisted, along with the final stiffening, at the resumption of heart activity. We speculate that efficacious blood perfusion of spinal cord and brainstem preceded that of cerebral cortex, producing a cortical–subcortical disconnection phenomenon, with complete loss of consciousness and persistence of motor activity. Physiological rhythmic movements, synchronous or alternating on both sides of the body, are innate motor behaviors generated by neural networks referred to as central pattern generators (CPGs), which contain the information for intersegmental coordination necessary for rhythmic motor patterns [9]. Location of CPGs is related to the motor behavior, being in the brainstem for chewing and respiration and in the spinal cord for walking, swimming, and hopping [10,11]. PBA in our patient closely resembled infant stepping, a prelocomotion alternating motor pattern, probably related to the activation of a spinal CPG generating independent walking [12]. We suggest that release of that CPG via anoxic cortical inactivation underlies the pathophysiology of bipedal activity related to the syncope in our case. Furthermore, epileptic bipedal activity might have a similar origin, with cortical inactivation related to the ictal discharge or ictal ignition of a cortical/subcortical CPG by way of corticofugal pathways. Nonparoxysmal stereotyped stepping has been reported in a stuporous man with meningoencephalitis and bilateral necrotic lesions in the medial frontoparietal cortices [13], a cortical zone that is an origin of epileptic seizures with PBA. Recurrent syncope as a complication or the presenting feature of neck malignancy, carotid body tumor included, is an uncommon but well-documented association [14]. The accepted mechanism implies abnormal afferent discharges from the carotid body causing excessive vagal activity. We excluded the diagnosis of frontal lobe epileptic seizures in our patient because of the initial lipothymic signs, subsequent complete loss of consciousness, and late symmetrical stiffening. Nocturnal frontal lobe epileptic seizures usually manifest with impairment of consciousness, no pallor and sweating, and asymmetrical dystonic posturing [1]. Moreover, no EEG epileptic activity was observed during the episode, and attacks completely subsided after removal of the carotid body tumor.
We suggest that different etiologies may underlie superimposable motor patterns with the mechanism of cortical/subcortical disconnection in conditions of altered vigilance. Extensive semiological and polygraphic studies of bipedal activity of various origins may contribute to clarification of this aspect. Ethical approval We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. A signed consent form authorizing publication has been obtained for the patient identified in the photographs accompanying this article. Conflict of interest None of the authors has any conflict of interest to disclose. Acknowledgment We are grateful to Ms. Alessandra Laffi for editing and secretarial assistance in preparing the article. References [1] Wada JA. Predominantly nocturnal recurrence of intensively affective vocal and facial expression associated with powerful bimanual, bipedal and axial activity as ictal manifestations of mesial frontal lobe epilepsy. Adv Epileptol 1989;17:261–7. [2] Lüders H, Acharya J, Baumgartner C, et al. Semiological seizure classification. Epilepsia 1998;39:1006–13. [3] Lempert T, Bauer M, Schmidt D. Syncope: a videometric analysis of 56 episodes of transient hypoxia. Ann Neurol 1994;36:233–7. [4] Iani C, Attanasio A, Manfredi M. Paroxysmal staring and masticatory automatisms during postural hypotension in a patient with multiple system atrophy. Epilepsia 1996;37:690–3. [5] Tassinari CA, Rubboli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias: a neuroethologic approach. Neurol Sci 2005;26(Suppl. 3):s225–32. [6] Macaluso GM, Guerra P, Di Giovanni G, Boselli M, Parrino L, Terzano GM. Sleep bruxism is a disorder related to periodic arousals during sleep. J Dent Res 1998;77:565–73. [7] Meletti S, Cantalupo G, Volpi L, Rubboli G, Magaudda A, Tassinari CA. Rhythmic teeth grinding induced by temporal lobe seizures. Neurology 2004;62:2306–9. [8] Chervin RD, Consens FB, Kutluay E. Alternating leg muscle activation during sleep and arousals: a new sleep-related motor phenomenon? Mov Disord 2003;35:551–9. [9] Grillner S. The motor infrastructure: from ion channels to neural networks. Nat Rev Neurosci 2003;4:573–86. [10] Nakamura Y, Katakura N. Generation of masticatory rhythm in the brainstem. Neurosci Res 1995;23:1–19. [11] Kiehn O, Kjaerulff O. Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 1998;16:110–29. [12] Yang JF, Lam T, Pang MY, Lamont E, Musselman K, Seinen E. Infant stepping: a window to the behaviour of the human pattern generator for walking. Can J Physiol Pharmacol 2004;82:662–74. [13] Sato S, Hashimoto T, Nakamura A, Ikeda S. Stereotyped stepping associated with lesions in the bilateral medial frontotemporal cortices. Neurology 2001;57:711–3. [14] Worth PF, Stevens JC, Lasri F, et al. Syncope associated with pain as the presenting feature of neck malignancy: failure of cardiac pacemaker to prevent attacks in two cases. J Neurol Neurosurg Psychiatry 2005;76:1301–3.