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Hemispheric predominance of abnormal findings in electroencephalogram (EEG)
Seizure 2002; 11: 442–444
doi:10.1053/seiz.2001.0642, available online at http://www.idealibrary.com on
Hemispheric predominance of abnormal findings in electroencephalogram (EEG) S. D. GATZONIS, S. ROUPAKIOTIS, E. KAMBAYIANNI, A. POLITI, N. TRIANTAFYLLOU, V. MANTOUVALOS, A. CHIONI, Ch. ZOURNAS & A. SIAFAKAS Department of Neurology, Athens Medical School, “Eginition” Hospital, Greece Correspondence to: S. D. Gatzonis, Department of Neurology, Athens Medical School, “Eginition” Hospital, 72 vas.Sofias av., Athens 11528, Greece. E-mail: [email protected]
The EEGs of 13 560 patients have been reviewed in order to determine whether abnormal findings, epileptiform or not, have a hemispheric dominance. We have included outpatients and hospitalized patients as well. Eight hundred and thirty-five EEGs had generalized abnormal findings, and 414 EEGs had lateralized abnormal findings. The EEGs of 322 patients (77.7%) had a left predominance, and those of 92 patients (22.3%) had a right predominance, of abnormal findings. A strong left predominance has been noted for the epileptiform discharges, i.e. 128 (79%) vs. 34 (21%). These results raise the possibility that the left hemisphere may be more vulnerable to nosological processes. c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.
Key words: Electroencephalography; brain asymmetry; cerebral lateralization; hemispheric dominance; specific EEG findings; EEG asymmetry.
INTRODUCTION Functional asymmetry has been a well-known phenomenon since the 19th century, as have in more recent times anatomic, cytoarchitectonic, developmental, maturation, reorganisation and chemical asymmetries between the two hemispheres 1 . Abnormal electroencephalographic patterns, especially the epileptiform ones, do not appear with equal frequency in both brain hemispheres, as might be expected, but there is most often a left lateralization, as reported in the literature 2, 3 . While this seems to be a long-standing observation, the systematic reviews trying to corroborate it are rare. We have conducted a retrospective study of a large series of the EEGs recorded in our laboratory over a period of 8 years (between Jan 1990 and May 1998). The aim of the study was to confirm the suggestion that there is a left predominance of epileptiform discharges and to find out if there is a predominance for the non-specific abnormal EEG findings. METHODS The EEG recordings of 13 560 patients (aged 16– 87 years, both outpatients and hospitalized ones), 1059–1311/02/070442 + 03
$35.00/0
were retrospectively examined. Routine EEG, EEG following sleep deprivation and EEG during druginduced sleep were done with three EEG-recorders, a 12-channel ALVAR reega 2000, a 16-channel ERA OTE biomedica, and an ELEMA-SCHONANDER 16-channel Mingograf. Twenty-one electrodes were placed according to the 10–20 system. In the 16channel machine, a monopolar and two dipolar montages (one longitudinal, one transverse) were recorded on paper. In the 12-channel machine, two longitudinal, two transverse and one monopolar montages were recorded. The recordings were classified depending on the presence of a lateral predominance of abnormalspecific or non-specific patterns. Spikes, spike-wave and polyspike-wave complexes, or sharp waves, clearly distinguished from the background activity, were considered to be specific patterns. All other abnormalities were considered as abnormal nonspecific patterns. Benign epileptiform transients of sleep, 6 s/wave, 14 and 6/s positive spikes, and wicket spikes were considered to be normal variants 4, 5 . The lateral predominance was confirmed when abnormalities were recorded: (1) exclusively from one hemisphere,
c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.
EEG predominance
443
(2) bilaterally, but with their amplitude in one hemisphere being at least double that in the other, or
(3) bilaterally, but with their frequency of appearance in one hemisphere being at least double that in the other 3, 4 .
Table 1: Aggregated EEG findings. EEG findings
Specific
Non-specific
Total
Generalized Left predominance Right predominance
130 128 34
705 194 63
835 322 97
Total
292
962
1254
The hypothesis was that, in EEGs with lateralization, one half of the lateralized abnormal findings had to have a right brain origin. The remaining one half had to be recorded from the left brain areas as the two hemispheres are morphologically identical. In order to detect significant departures of the percentages counted for each group from their normal value of 50%, one-sample test for a binomial proportion was employed. All tests were considered to be significant at 0.05. Three age-groups were examined because of the different proportions of diseases across the agegroups.
RESULTS Among a total of 13 560 patients examined, abnormal recordings were detected in 1254 (687 male (M), 567 female (F)). Generalized specific patterns appeared in 130 patients (57 M, 73 F) whereas generalized non-specific findings appeared in 705 patients (404 M, 301 F) (Table 1). Lateral predominance was revealed in 419 EEGs, of which 322 (77 %, 178 M, 124 F) showed left hemisphere predominance and 97 (23 %), 48 M, 49 F) showed right predominance. Of the 322 EEGs with the left lateralization, specific epileptiform patterns were disclosed in 128 (64 M, 64 F) while non-specific findings were disclosed in 194 (114 M, 80 F). Of the 97 EEGs lateralized to the right, specific and nonspecific findings were disclosed in 34 (13 M, 21 F) and 63 (35 M, 28 F) respectively (Table 2). Statistical analysis demonstrated a significant difference in the left side dominance for specific and nonspecific abnormal findings, for both genders and for all three age-groups.
DISCUSSION It has been reported in the literature that abnormalities, recorded in EEGs, are most often disclosed, predominantly with a left lateralization. For instance, two-thirds of 4032 patients studied by Paolozzi 2 were proved to have abnormal patterns in the left hemisphere (no mention is made about the specificity of those patterns). The left hemisphere’s tumours, per se, more often cause seizures than the right one’s 6 . Dean et al. 3 reported that in EEGs with epileptic activity, 70% of the recordings present this activity predominantly in the left hemisphere. There is also a predominance of right cerebral palsy 7–9 . Our sample comprised both epileptic patients and patients with various other neurological disorders and in the abnormal EEGs, three-fourths of both specific and non-specific findings were lateralized to the left in accordance with the above results. The predominance of abnormal findings in the left was statistically significant in both the sexes and all the age-groups mentioned above. The reason for this discrepancy can only be speculated. It has been suggested that the presence of the language centres in the left hemisphere (in the majority of right-handed people) causes more obvious clinical signs and leads these patients to the attention of a physician earlier 1, 3 . Although, it is evident that right-sided lesions would present their symptomatology at a relatively later stage, they should be expected, nevertheless, to draw the attention of the patients, their relatives, or a physician, eventually. This speculation cannot explain the discrepancy between the EEG findings from the two hemispheres. Because the right-sided lesion was noticed later, a more extensive brain area would be affected, producing more detectable electrical abnormalities. Consequently, the discrepancy between the EEG findings from the two hemispheres, should be attributed to their inherent structural and functional organisation which presumably leads to the formation of more ‘silent’ or ‘redundant’ areas that are less likely to present symptoms, ever. The left hemisphere maturates later than the right 1, 10 , and thus remains exposed to harmful agents for longer periods. The more sophisticated functions represented in the left hemisphere (such as language and recognition) probably reflect a more complicated and, consequently, more vulnerable structure 1, 11 . The developmental and organisational differences between the hemispheres can be inferred by: 1. the asymmetrical levels of expression of signal molecules during the nervous system’s development and differentiation; 2. the asymmetries in various brain structures; and
444
S. D. Gatzonis et al.
Table 2: EEG findings according to sex- and age-groups. EEG findings
Male
Female
Total
Age < 25 years
Age 25–50 years
Age > 50 years
Generalized specific Generalized non-specific Left hem. specific Left hem. non-specific Right hem. specific Right hem. non-specific
57 404 64 114 13 35
73 301 64 80 21 28
130 705 128 194 34 63
47 135 38 39 13 14
50 241 41 88 12 21
33 329 49 67 9 28
Total
687
567
1254
286
453
515
3. the differential localisation and expression of neurotransmitters, such as GABA, dopamine, acetylcholine and their receptors, which could lead to differential synaptic organisation and different epileptic thresholds as Dean et al. have proposed 3 . They were based mainly on the higher likelihood of left-side than right-side tumours to produce seizures, on differential expression of neurotransmitters 13 , and on lateralization of carbamazepine efficacy 14 . In conclusion, our results confirm that abnormal EEG findings have most often (in 78% of cases) a left lateralization. A couple of suggestions could be discussed in the light of information regarding the brain asymmetry. A more potent liability to nosological processes for the left hemisphere seems to be a possible explanation.
REFERENCES 1. Geschwind N. and Galaburda A. M. Cerebral lateralization, biologic mechanisms, associations and pathology. I. A hypothesis and a program for research. Archives of Neurology 1985; 42: 428–459. 2. Paolozzi C. Hemispheric dominance and asymmetry related to vulnerability of cerebral hemispheres. Acta Neurologica 1969; 24: 13–28. 3. Dean A., Solomon G., Harden S., Papakostas G. and Labar D. Left hemispheric dominance of epileptiform discharges. Epilepsia 1997; 38: 503–505.
4. Salinsky M., Kanter R. and Dasheiff R. M. Effectiveness of multiple EEGs in supporting the diagnosis of epilepsy: an operational curve. Epilepsia 1987; 28: 331–334. 5. Wastemorland B. F. Benign EEG variants and patterns of uncertain clinical significance. In: Current Practice of Clinical Electroencephalography. 2nd Edition, (Eds D. Daly and T. Pedley). New York, Raven Press, 1990: pp. 243–252. 6. Foy P. M., Chadwick D. W., Rajgopalan N., Johnson A. L. and Shaw M. D. M. Do anticonvulsant drugs alter the pattern of seizures after craniotomy? Journal of Neurology, Neurosurgery and Psychiatry 1992; 55: 753–757. 7. Goodman R. Childhood hemiplegia: is the side of the lesion influenced by a family history of left-handedness? Developmental Medicine and Child Neurology 1994; 36: 406–411. 8. Kurban K. C. K. and Leviton A. Cerebral palsy. New England Journal of Medicine 1994; 330: 188–194. 9. Uvebrand P. Hemiplegic cerebral palsy, aetiology and outcome. Acta Pediatrica Scandinavica (Supplement) 1988; 345: 1–100. 10. Taylor D. C. Differential rates of cerebral maturation between sexes and between hemispheres. Lancet 1969; 2: 140–142. 11. Galaburda A. M., Sanides F. and Geschwind N. Human brain: cytoarchitectonic left-right asymmetries in the temporal speech region. Archives of Neurology 1978; 35: 812–817. 12. Amaducci L., Sorbi S., Albanese A. and Gainotti G. Choline acetyl-transferase activity differs in right and left human temporal lobes. Neurology 1981; 31: 799–805. 13. Glick S. D., Ross D. A. and Hough L. B. Lateral asymmetries of neurotransmitters in human brain. Brain Research 1982; 234: 53–63. 14. Defazio G., Lepore V., Speccio L. M., Pisani F. and Livrea P. The effect of electroencephalographic focus laterality on efficacy of carbamazepine in complex partial and secondarily generalised tonic–clonic seizures. Epilepsia 1991; 32: 706–711.
doi:10.1053/seiz.2001.0642, available online at http://www.idealibrary.com on
Hemispheric predominance of abnormal findings in electroencephalogram (EEG) S. D. GATZONIS, S. ROUPAKIOTIS, E. KAMBAYIANNI, A. POLITI, N. TRIANTAFYLLOU, V. MANTOUVALOS, A. CHIONI, Ch. ZOURNAS & A. SIAFAKAS Department of Neurology, Athens Medical School, “Eginition” Hospital, Greece Correspondence to: S. D. Gatzonis, Department of Neurology, Athens Medical School, “Eginition” Hospital, 72 vas.Sofias av., Athens 11528, Greece. E-mail: [email protected]
The EEGs of 13 560 patients have been reviewed in order to determine whether abnormal findings, epileptiform or not, have a hemispheric dominance. We have included outpatients and hospitalized patients as well. Eight hundred and thirty-five EEGs had generalized abnormal findings, and 414 EEGs had lateralized abnormal findings. The EEGs of 322 patients (77.7%) had a left predominance, and those of 92 patients (22.3%) had a right predominance, of abnormal findings. A strong left predominance has been noted for the epileptiform discharges, i.e. 128 (79%) vs. 34 (21%). These results raise the possibility that the left hemisphere may be more vulnerable to nosological processes. c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.
Key words: Electroencephalography; brain asymmetry; cerebral lateralization; hemispheric dominance; specific EEG findings; EEG asymmetry.
INTRODUCTION Functional asymmetry has been a well-known phenomenon since the 19th century, as have in more recent times anatomic, cytoarchitectonic, developmental, maturation, reorganisation and chemical asymmetries between the two hemispheres 1 . Abnormal electroencephalographic patterns, especially the epileptiform ones, do not appear with equal frequency in both brain hemispheres, as might be expected, but there is most often a left lateralization, as reported in the literature 2, 3 . While this seems to be a long-standing observation, the systematic reviews trying to corroborate it are rare. We have conducted a retrospective study of a large series of the EEGs recorded in our laboratory over a period of 8 years (between Jan 1990 and May 1998). The aim of the study was to confirm the suggestion that there is a left predominance of epileptiform discharges and to find out if there is a predominance for the non-specific abnormal EEG findings. METHODS The EEG recordings of 13 560 patients (aged 16– 87 years, both outpatients and hospitalized ones), 1059–1311/02/070442 + 03
$35.00/0
were retrospectively examined. Routine EEG, EEG following sleep deprivation and EEG during druginduced sleep were done with three EEG-recorders, a 12-channel ALVAR reega 2000, a 16-channel ERA OTE biomedica, and an ELEMA-SCHONANDER 16-channel Mingograf. Twenty-one electrodes were placed according to the 10–20 system. In the 16channel machine, a monopolar and two dipolar montages (one longitudinal, one transverse) were recorded on paper. In the 12-channel machine, two longitudinal, two transverse and one monopolar montages were recorded. The recordings were classified depending on the presence of a lateral predominance of abnormalspecific or non-specific patterns. Spikes, spike-wave and polyspike-wave complexes, or sharp waves, clearly distinguished from the background activity, were considered to be specific patterns. All other abnormalities were considered as abnormal nonspecific patterns. Benign epileptiform transients of sleep, 6 s/wave, 14 and 6/s positive spikes, and wicket spikes were considered to be normal variants 4, 5 . The lateral predominance was confirmed when abnormalities were recorded: (1) exclusively from one hemisphere,
c 2002 Published by Elsevier Science Ltd on behalf of BEA Trading Ltd.
EEG predominance
443
(2) bilaterally, but with their amplitude in one hemisphere being at least double that in the other, or
(3) bilaterally, but with their frequency of appearance in one hemisphere being at least double that in the other 3, 4 .
Table 1: Aggregated EEG findings. EEG findings
Specific
Non-specific
Total
Generalized Left predominance Right predominance
130 128 34
705 194 63
835 322 97
Total
292
962
1254
The hypothesis was that, in EEGs with lateralization, one half of the lateralized abnormal findings had to have a right brain origin. The remaining one half had to be recorded from the left brain areas as the two hemispheres are morphologically identical. In order to detect significant departures of the percentages counted for each group from their normal value of 50%, one-sample test for a binomial proportion was employed. All tests were considered to be significant at 0.05. Three age-groups were examined because of the different proportions of diseases across the agegroups.
RESULTS Among a total of 13 560 patients examined, abnormal recordings were detected in 1254 (687 male (M), 567 female (F)). Generalized specific patterns appeared in 130 patients (57 M, 73 F) whereas generalized non-specific findings appeared in 705 patients (404 M, 301 F) (Table 1). Lateral predominance was revealed in 419 EEGs, of which 322 (77 %, 178 M, 124 F) showed left hemisphere predominance and 97 (23 %), 48 M, 49 F) showed right predominance. Of the 322 EEGs with the left lateralization, specific epileptiform patterns were disclosed in 128 (64 M, 64 F) while non-specific findings were disclosed in 194 (114 M, 80 F). Of the 97 EEGs lateralized to the right, specific and nonspecific findings were disclosed in 34 (13 M, 21 F) and 63 (35 M, 28 F) respectively (Table 2). Statistical analysis demonstrated a significant difference in the left side dominance for specific and nonspecific abnormal findings, for both genders and for all three age-groups.
DISCUSSION It has been reported in the literature that abnormalities, recorded in EEGs, are most often disclosed, predominantly with a left lateralization. For instance, two-thirds of 4032 patients studied by Paolozzi 2 were proved to have abnormal patterns in the left hemisphere (no mention is made about the specificity of those patterns). The left hemisphere’s tumours, per se, more often cause seizures than the right one’s 6 . Dean et al. 3 reported that in EEGs with epileptic activity, 70% of the recordings present this activity predominantly in the left hemisphere. There is also a predominance of right cerebral palsy 7–9 . Our sample comprised both epileptic patients and patients with various other neurological disorders and in the abnormal EEGs, three-fourths of both specific and non-specific findings were lateralized to the left in accordance with the above results. The predominance of abnormal findings in the left was statistically significant in both the sexes and all the age-groups mentioned above. The reason for this discrepancy can only be speculated. It has been suggested that the presence of the language centres in the left hemisphere (in the majority of right-handed people) causes more obvious clinical signs and leads these patients to the attention of a physician earlier 1, 3 . Although, it is evident that right-sided lesions would present their symptomatology at a relatively later stage, they should be expected, nevertheless, to draw the attention of the patients, their relatives, or a physician, eventually. This speculation cannot explain the discrepancy between the EEG findings from the two hemispheres. Because the right-sided lesion was noticed later, a more extensive brain area would be affected, producing more detectable electrical abnormalities. Consequently, the discrepancy between the EEG findings from the two hemispheres, should be attributed to their inherent structural and functional organisation which presumably leads to the formation of more ‘silent’ or ‘redundant’ areas that are less likely to present symptoms, ever. The left hemisphere maturates later than the right 1, 10 , and thus remains exposed to harmful agents for longer periods. The more sophisticated functions represented in the left hemisphere (such as language and recognition) probably reflect a more complicated and, consequently, more vulnerable structure 1, 11 . The developmental and organisational differences between the hemispheres can be inferred by: 1. the asymmetrical levels of expression of signal molecules during the nervous system’s development and differentiation; 2. the asymmetries in various brain structures; and
444
S. D. Gatzonis et al.
Table 2: EEG findings according to sex- and age-groups. EEG findings
Male
Female
Total
Age < 25 years
Age 25–50 years
Age > 50 years
Generalized specific Generalized non-specific Left hem. specific Left hem. non-specific Right hem. specific Right hem. non-specific
57 404 64 114 13 35
73 301 64 80 21 28
130 705 128 194 34 63
47 135 38 39 13 14
50 241 41 88 12 21
33 329 49 67 9 28
Total
687
567
1254
286
453
515
3. the differential localisation and expression of neurotransmitters, such as GABA, dopamine, acetylcholine and their receptors, which could lead to differential synaptic organisation and different epileptic thresholds as Dean et al. have proposed 3 . They were based mainly on the higher likelihood of left-side than right-side tumours to produce seizures, on differential expression of neurotransmitters 13 , and on lateralization of carbamazepine efficacy 14 . In conclusion, our results confirm that abnormal EEG findings have most often (in 78% of cases) a left lateralization. A couple of suggestions could be discussed in the light of information regarding the brain asymmetry. A more potent liability to nosological processes for the left hemisphere seems to be a possible explanation.
REFERENCES 1. Geschwind N. and Galaburda A. M. Cerebral lateralization, biologic mechanisms, associations and pathology. I. A hypothesis and a program for research. Archives of Neurology 1985; 42: 428–459. 2. Paolozzi C. Hemispheric dominance and asymmetry related to vulnerability of cerebral hemispheres. Acta Neurologica 1969; 24: 13–28. 3. Dean A., Solomon G., Harden S., Papakostas G. and Labar D. Left hemispheric dominance of epileptiform discharges. Epilepsia 1997; 38: 503–505.
4. Salinsky M., Kanter R. and Dasheiff R. M. Effectiveness of multiple EEGs in supporting the diagnosis of epilepsy: an operational curve. Epilepsia 1987; 28: 331–334. 5. Wastemorland B. F. Benign EEG variants and patterns of uncertain clinical significance. In: Current Practice of Clinical Electroencephalography. 2nd Edition, (Eds D. Daly and T. Pedley). New York, Raven Press, 1990: pp. 243–252. 6. Foy P. M., Chadwick D. W., Rajgopalan N., Johnson A. L. and Shaw M. D. M. Do anticonvulsant drugs alter the pattern of seizures after craniotomy? Journal of Neurology, Neurosurgery and Psychiatry 1992; 55: 753–757. 7. Goodman R. Childhood hemiplegia: is the side of the lesion influenced by a family history of left-handedness? Developmental Medicine and Child Neurology 1994; 36: 406–411. 8. Kurban K. C. K. and Leviton A. Cerebral palsy. New England Journal of Medicine 1994; 330: 188–194. 9. Uvebrand P. Hemiplegic cerebral palsy, aetiology and outcome. Acta Pediatrica Scandinavica (Supplement) 1988; 345: 1–100. 10. Taylor D. C. Differential rates of cerebral maturation between sexes and between hemispheres. Lancet 1969; 2: 140–142. 11. Galaburda A. M., Sanides F. and Geschwind N. Human brain: cytoarchitectonic left-right asymmetries in the temporal speech region. Archives of Neurology 1978; 35: 812–817. 12. Amaducci L., Sorbi S., Albanese A. and Gainotti G. Choline acetyl-transferase activity differs in right and left human temporal lobes. Neurology 1981; 31: 799–805. 13. Glick S. D., Ross D. A. and Hough L. B. Lateral asymmetries of neurotransmitters in human brain. Brain Research 1982; 234: 53–63. 14. Defazio G., Lepore V., Speccio L. M., Pisani F. and Livrea P. The effect of electroencephalographic focus laterality on efficacy of carbamazepine in complex partial and secondarily generalised tonic–clonic seizures. Epilepsia 1991; 32: 706–711.