A Survey of Epileptic Disorders in bouthwest Prance: 3euures in Elderly Patients J&me
Loiseau, MD," Pierre Loiseau, MD," Bernard Duchk, MD,' Martine Guyot, MD," Jean-Franfois Dartigues, MD,'? and Bruno Aublet, MDt ~~
An underestimation of epileptic seizures occurring in aged patients is likely. In an epidemiological survey undertaken in Southwest France, the annual incidence rate per 100,OOO persons 60 years or older was 127.2 for all seizures (101.3 in persons aged 60 to 69, 150.4 in those aged 70 to 79, and 139.9 in persons 80 years or older). It was 34.1 for symptomatic localization-related and undetermined epilepsies, 16.1 for isolated seizures, and 77.0 for seizures related to an acute situation, such as metabolic derangements, stroke, or head trauma. In this survey, seizures with an onset age of 60 or older represented 28.0% of the confirmed epilepsies, 17.5% of the isolated seizures, and 52.6% of the acute symptomatic seizures. These figures differ dramatically from those in most previous reports concluding that age-specific incidence declined through adult life. They are closer to the data from more recent reports. The main reason for such a high incidence of epileptic seizures in elderly patients is the number of acute symptomatic (or situation-related) seizures. However, even chronic epilepsies increase in frequency in aging persons. Cerebrovascular disease was the most frequently recognized origin (53.9% of the patients with confirmed epilepsies) and brain tumor was found in 32.9% of the patients. Loiseau J, Loiseau P, Duch6 B, Guyot M, Dartigues J-F, Aublet B. A survey of epileptic disorders in southwest France: seizures in elderly patients. Ann Neurol 1990;27:232-237
Methods
It is generally accepted that about 75% of epilepsies begin before the age of 20 years. This figure, given by Gowers [l} and later by Lennox and Lennox 121, has been confirmed in classic epidemiological surveys. It has been also stated that after age 20 age-specific incidence declines to a rather low level that remains fairly constant throughout adult life or decreases in each subsequent decade of age 13-61. The onset of a seizure disorder in the elderly is held to be rare. In aged patients, nonepileptic fits (i.e., syncopal attacks) are considered much more frequent than epileptic seizures (81% versus 14%, respectively C71). However, in more recent years, the occurrence of epileptic seizures in the elderly has been considered less rare [S]. Agespecific incidence increases in the last decades of life 191 and is more than 100 per 100,000 1101. A large body of literature exists concerning the origins of epileptic seizures in the elderly. Very different figures have been published 1111. The aim of our study was to evaluate the incidence and causes of epileptic seizures in persons 60 years or older.
The present study is part of an epidemiological survey undertaken in Southwest France. The population at risk resided in the department of Gironde, an administrativedistrict around Bordeaux. In a 1982 census there were 1,128,164 residents, 223,224 of whom were 60 years or older. Eligible persons were all those who experienced the first epileptic seizure of their life during the period of March 1, 1984, to February 28, 1985, and who came to medical attention. As the Gironde population increases very slowly, the 1982 census gave a fair estimate of the 1984 population. Data were prospectively collected by all the neurologists and electroencephalographersof the department and bordering towns. Information available from the cards they completed included name, address, date of birth, sex, history of illness, age at onset of symptoms, description of seizures, possible cause, physical and neurological findings, and date and results of electroencephalograms (EEGs) and of computed tomographic (CT) scanning. A retrospective complementary survey was made in the hospital neurology departments. All data were reviewed by us. Further information was obtained by examining medical records and by further questioning patients, family, or patients' physicians during the follow-up
From the "Department of Neurology, University Hospital, Bordeaux, and tDepartment of Epidemiology, University of Bordeaux, Bordeaux, France.
Received Apr 17, 1989, and in revised form Aug 8. Accepted for publication Aug 9, 1989. Address correspondence to Dr Loiseau, Hopital Pellegrin, 33076 Bordeaux, France.
232 Copyright 0 1990 by the American Neurological Association
period. The difficulties and biases of the survey will be discussed in another paper El la]. They are mainly related to the case ascertainment method: Even in Southwest France, which has a very high number of physicians, we are not sure that all patients come to medical attention after a first seizure. An underestimation is even more likely in elderly patients than in children or young adults. Seizures are often poorly described by elderly persons. A classification according to seizure type would be of dubious value. It was easier and more precise to consider epileptic syndromes. An epileptic syndrome is an epileptic disorder characterized by a cluster of signs and symptoms customarily occurring together 1121. According to the proposal for a classification of epilepsies and epileptic syndromes made by the Commission on Classification and Terminology of the International League against Epilepsy [121, four epileptic syndromes are found in aged patients. 1. Symptomatic localization-related epilepsies: Diagnosis is based on any sign or symptom of anatomical localization (i.e., partial seizures or EEG or CT signs of localization). A first subgroup corresponds to remote symptomatic seizures { 131. Seizures occur in patients with a history of central nervous system insult that is thought to be associated with an increased risk of epilepsy when the lapse of time between the insult and the first seizure is more than 1 week. Patients presenting such etiological evidence were considered epileptic even if they had experienced only one seizure at the time of diagnosis. Patients with no known cerebral insult and with no focal abnormalities on CT scan constituted the second subgroup. They were accepted as epileptic only when they had experienced more than one focal seizure at the time of first referral to a specialist. 2. Undetermined epilepsies: This category covers all patients without unequivocal generalized or focal seizures and without etiological factors. Patients had to have experienced more than one seizure at the time of referral. 3. Isolated, apparently unprovoked epileptic events: This category includes patients with isolated seizures, either partial or generalized, without EEG- or CT-detected abnormalities, and without etiological factors. 4. Situation-related seizures: These were named acute symptomatic seizures by Hauser and colleagues [ 131. Others have called them provoked seizures. They are associated with metabolic disorders, alcohol consumption or withdrawal, central nervous system infection, stroke, or head trauma within 7 days of the onset of seizures. They are often but not necessarily isolated epileptic events. Some patients experience several seizures during a unique acute illness. Some patients present with repeated seizures, each related to a recurrent acute situation (i.e., hypoglycemia or alcohol).
The following criteria were used for identification of etiological factors in symptomatic localization-related epilepsies and situation-related seizures:
1. Cerebrovascular disease: either unequivocal evidence of a remote or a recent stroke or subarachnoid hemorrhages, diagnosed either on clinical grounds or CT scanning, or clear evidence of hemodynamic disturbances sufficient for modifying cerebral blood flow. (All patients of the latter group were considered as having had situation-related seizures.) 2. A severe head trauma for remote symptomatic seizures, and any head trauma for acute symptomatic seizures. 3. CT evidence of brain tumor. 4. A documented metabolic disorder with marked electrolyte or glycemic abnormalities. 5. Acute abuse or withdrawal of alcohol in chronic alcoholic patients. 6. Clinical and neuropsychological signs of dementia. 7. Symptoms and signs of meningitis or encephalitis.
Results Two hundred and eighty-four patients were accepted for the study. The annual incidence rate for all seizures (whatever their category) was 127.2 per 100,000 persons 60 years or older. Age-specific and sex-specific incidence rates for all seizures are presented in Table 1. Incidence rates increased with age and were significantly higher for men. Table 2 presents annual incidence rates by type of epileptic syndrome and by sex. Situation-related seizures (i.e., acute symptomatic seizures) were the most frequent. For three of the syndromes, the incidence rate was higher for men. In the present survey, among 804 patients considered as having had a first nonfebrile seizure during the recording period, 284 were 60 years or older. They represent 28.0% of the confirmed epilepsies, 17.5% of the isolated seizures, and 52.6% of the acute symptomatic seizures in the total sample. Table 3 presents annual incidence rates by type of epileptic syndrome and by age groups. Only the incidence for situation-related seizures increased with age. A cause of seizure could be identified in 68 patients with spontaneous seizures (Table 4). By definition, undetermined epilepsy (2 patients) and isolated seizures (36 patients) have no known cause. Cerebrovascular
Table I . Age and Sex-Specifc Annual Incidence Rate of Seizures in Elderly Patients per 100,000 Population Men
Women
Total
Age (yr)
No.
Population
Rate
No.
Population
Rate
No.
Population
Rate
60-69 70-79 80 + Total
65 65 26 156
43,952 33,421 12,876 90,248
147.9 194.5 201.9 172.8
32 60 36 128
5 1,792 49,7 12 31,472 132,976
61.8 120.7 114.4 96.2
97 125 62 284
95,744 83,132 44,348 223,224
101.3 150.4 139.9 127.2
Loiseau et al: Seizures in Elderly Patients
233
Table 2. Sex-SpecificAnnual Incidence Rate of Epileptic Syndromes in Patients Aged 60 or Older per 100,000 Population Men
Symptomatic localization-related epilepsies Undetermined epilepsies Isolated seizures Situation-related seizures
Total
Women
No.
Rate
No.
Rate
No.
Rate
51
56.5 0.0 23.3 93.1
23 2 15 88
17.3 1.5 11.3 66.2
74 2 36 172
33.2 0.9 16.1 77.0
0
21 84
Table 3. Age-SpecificAnnual Incidence Rate of Epileptic Syndromes in Elderb Patients per 100,000 Population Symptom LocalizationRelated Epilepsies
Undetermined Epilepsies
SituationRelated Seizures
Isolated Seizures
Age (Y r)
Population
No.
Rate
No.
Rate
No.
Rate
No.
Rate
60-69 70-79 80 +
95,744 83,132 44,348
34 31 9
35.5 37.3 20.3
1 0 1
1.0 0.0 2.2
14 15 7
14.6 18.0 15.8
48 79 45
50.1 95.0 101.5
disease was the most frequently recognized origin, found in 36.6% of patients with spontaneous seizures and in 53.9% of patients with confirmed epilepsy. Its sex-specific incidence rate was significantly higher in men. Sixty-two (66.7%) of the 93 patients who had seizures within the acute phase of a stroke died-13 within the first week, 17 within the first month, 14 within the first 6 months, 8 within the first year, and 10 within 3 years after stroke. Among our 41 patients with late vascular epilepsy, 30 had ischemic lesions and 3 had sequelae of hematoma. The nature of the lesion was not documented in the other 8 patients. A brain tumor was found in 22.3% of patients with spontaneous seizures, representing a similar percentage of etiological factor in both sexes, but with an incidence 4 times higher in men. Ten patients had glioblastoma and 11 had metastasis. Situation-related seizures (Table 5) had a vascular origin in half of the patients. They were associated with stroke in 56 patients and with cardiac failure in 37 atherotic patients. Toxic seizures were more frequent in number and in incidence in men because they were mainly alcohol related.
Discussion In an epidemiological survey, one of the major difficulties is deciding what to include. Epilepsy is characterized by the occurrence of at least two unprovoked seizures separated by a greater than 24-hour interval. We referred to this as confirmed epilepsy and added to this group a few patients who had experienced only one seizure at the time of referral but who had a high risk of recurrence. Patients who have an accidental or a 234 Annals of Neurology Vol 27 No 3 March 1990
situation-related seizure will not necessarily develop other seizures. Obviously, they are different from those having chronic epilepsy. However, these patients may require specific investigation, treatment, and care E14). Hence, they are important from an epidemiological viewpoint. A nice solution was chosen by Hauser and Kurland 191. They classdied cases of seizures in four categories: (1) recurrent epileptic attacks; (2) single epileptic attack without known cause; (3) single or multiple seizures, each associated with an acute illness; and (4) febrile convulsions. The 1989 proposal for the classification of epileptic syndromes 112) affords another solution, since all patients without recurrent seizures may be included under the heading of special syndromes. When all the seizures (isolated or recurrent unprovoked seizures and situation-related seizures) are considered, an annual incidence rate of 127.2 per 100,000 persons aged 60 years or older differs dramatically from the rates of other studies 115-171. In one instance it was found to be 33 per 100,000 fl81. However, Luhdorf and colleagues {lo) in Denmark retrospectively studied the incidence of epileptic seizures in persons who were older than 60 years and who were admitted to a hospital that received virtually all patients from the region. They assumed that practically all the elderly with fits were diagnosed. The incidence rate and age curve for patients presenting with a first seizure during the study period were very similar to ours: The mean annual incidence rate per 100,000 at 60 years or older was 104; incidence rates in the age ranges 60 to 64, 65 to 69, 70 to 74, 75 to 79, and 80 and older were 79, 111, 131, 123, and 76, respec-
Table 4. Cause of Symptomatic Localization-Related Epilepsies in 284 Patients with First Seizure at Age 60 or Older
Men Origin
No.
Incidence Rate
Vascular Tumor Traumatic Unknown Total
27 18 1
29.9 19.9 1.1
5
5.5
51
56.5
Women
Total
%
No.
Incidence Rate
%
No.
Rate
%
52.9 35.3 2.0 9.8 100
14 7 1 1 23
10.5 5.3 0.8 0.8 17.3
60.9 30.4 4.3 4.3 100
41 25 2 6 74
18.4 11.2 0.9 2.7 33.2
55.4 33.8 2.7 8.1 100
Incidence
Table 5 . Cause of Situation-Related Seizures in 284 Patients with First Seizure at Age 60 or Older
Men Origin
No.
Vascular Metabolic Toxic Dementia Traumatic Infection Total
42 12 18 4
6 2 84
Women
Total
Incidence
Incidence Rate
%
No.
Rate
46.5 13.3 19.9 4.4 6.6 2.2 93.1
50.0 14.3 21.4 4.8 7.1 2.4 100
51 14 7 12 1 3
38.4 10.5 5.3 9.0 0.7 2.2 66.2
88
tively. They included all first seizures, either spontaneous or provoked. When only definite cases of epilepsy were considered, the incidence rate was 77 per year per 100,000 persons at age 60 or older. Concerning the age- and sex-specific incidences of the various epileptic syndromes in patients 60 years or older (see Table 2), some comments may be made. First of all, the main reason for so high an incidence of epileptic seizures in elderly patients was the number of acute symptomatic seizures. Secondly, the situationrelated seizure rate increased dramatically after the age of 70 (see Table 3). The rate for confirmed epilepsy was much higher in men than in women, whereas the rate of acute symptomatic seizures was not very different between sexes. Isolated seizures occupied an intermediate position. As for confirmed epilepsy, our figure is once more very different from previously reported ones. Annual incidence rate for confirmed epilepsy in persons aged 60 or older was found to be 6.2 per 100,000 151 or 15 per 100,000 1191, 15.7 per 100,000 for persons aged 60 to 69 and 7.6 per 100,000 for 70 or older 141, and 17 per 100,000 for persons aged 60 to 69 and 12 per 100,000 for 70 or older C61. However, our data are less impressive than that of Hauser and Kurland [91, who reported an incidence rate of 82.0 per 100,000 in patients older than 60 during the period 1965 to 1967. This is probably due to a longer follow-up period at the Mayo Clinic, with recurrence of seizures over time. However, their incidence of
% 58.0 15.9 8.0 13.6 1.1 3.4 100
No.
Incidence Rate
%
93 26 25 16 7 5 172
41.7 11.6 11.2 7.2 3.1 2.2 77.0
54.1 15.1 14.5 9.3 4.1 2.9 100
isolated spontaneous or provoked convulsive disorders (69.4/100,000 131) was lower than ours, but the authors expected a marked underestimation in this category due to their case-record system. Vascular disease is generally considered a prominent cause of seizures in the elderly. However, its etiological position has been diversely estimated: 4% 1201, 17% 1211, 18% 1221, 26% 1231, 28% 1241, 32% 1111, 42% 1251, 43% 126, 271, 50% C81, 52% 1281, and 69.2% r29). The problem arises from the various meanings given to the term vascakzr disease. Either in the acute phase of a cerebral infarct or intracranial bleeding or long after it, postapoplectic seizures are a well-defined entity. Only these seizures were taken into account by some [ l l , 241. But other authors assumed that nonspecific extracerebral atherosclerosis may cause epilepsy on the assumption that systemic vascular disease is associated with cerebrovascular disease. This assumption has been considered rather speculative 1113. However, De Reuck 1301 expressed doubts as to whether vascular epilepsy can be the result of the presence of a cerebral infarct alone and stressed the importance of additional exogenous factors, such as hypertensive episodes, periods of cardiac failure, or respiratory or metabolic disorders. For this reason, we distinguished two forms of seizures of acute vascular origin: clearly postapoplectic seizures and seizures occurring during severe hemodynamic disturbances. Seizures at the onset of stroke have a practical Loiseau et al: Seizures in Elderly Patients 235
interest. It is widely held that patients who have seizures within the acute phase of a stroke have a poor prognosis 131-34). The proportion of epileptogenic brain tumors in elderly patients differs widely between studies, ranging from 2 to 28% (see {ll))according to the source of data (neurosurgeons, neurologists, electroencephalographers, internists, inpatients or outpatients, and so on) and to the inclusion criteria (absence or presence of neurological symptoms other than epilepsy). Most of the tumors found in elderly patients were malignant 111, 22). In some studies cerebral atrophy shown by CT has been considered an etiological factor 111, 351. We share the opinion expressed by Shorvon and colleagues 136): It is quite common in elderly persons, without any correlation with neurological status. It cannot be considered a causative factor in epileptic disorders. The proportion of patients with an unknown cause differs according to whether all spontaneous seizures (n = 112) or confirmed epilepsy only (n = 76) are considered (39.3% versus 10.596, respectively). A follow-up period with recurrence of isolated cryptogenic seizures would modify these figures. The published data for epilepsies with an onset in patients older than 50 in whom no etiological factor is found are 50% 121, 241, 28% E81, 25% 1111, 22% 1371, or 16% 138). The introduction of CT scanning and magnetic resonance imaging lowered the percentage of late-onset epilepsy with unknown cause. Unsuspected cerebral infarcts can provoke seizures with no recognizable stroke 136, 38-41). Situation-related seizures need no further comment except on their frequency. Because an important effort was made to detect them, they are more numerous in this study than in series reported from neurological centers. The underlying illness is the dominant clinical feature. It is easily recognized and the patient is not referred for further investigation. Some seizures probably escape medical attention. Seizures in demented patients are not rare 18, 25, 383 but are often single events in patients with metabolic derangements. For this reason, they were included in the group of situation-related seizures. This study was supported in part by Sanofi, Synthelabo, and the Direction Rkgionale des Affaires Sanitaires et Sociales of Aquitaine. We thank Drs M. Aupy, A. Banayan, CI. Bensch, D. Bequet, A. Biolsi, J. Bourdot, F. Bretegnier, P. Chavois, S. Cohadon, D. Daynes, F. X. Debelleix, M. M. Deliac, F. Dutertre, A. Fournier, J. P. Girard, T. Herbelleau, M. Jogeix, A. Laporte, J. L. Larrieu, M. Legroux, F. Maupetit, J. Paty, M. Pestre, V. Riemens, J. Rozier, J. Saintarailles,E. Sauvan-Vian, F. Terraz, C1. Villeneuve-Bugat, and J. D. Vincent for their kind assistance in collecting data. We are grateful to P. L. Morselli, MD (LERS-Synthelabo), A. Perret, MD (Sanofi), and G. Venaud, M D (Labaz, France), for their help.
236 Annals of Neurology Vol 27 No 3 March 1990
We would also like to thank the doctors in public and private practice who were willing to participate in this survey. We wish to acknowledge Dominique Nicolini for typing and Jim Sneed for assisting in preparation of the manuscript.
References 1. Gowers WR. Epilepsy and other chronic convulsive diseases. New York: William Wood, 1885 2. Lennox WG, Lennox MA. Epilepsy and related disorders, vol 1. Boston: Little, Brown, 1960 3. Crombie DL, Cross KV, Fry J, et al. A survey of the epilepsies in general practice. A report by the research committee of the College of General Practitioners. Br Med J 1960;2:416-422 4. Brewis M, Poskanzer DC, Rolland C, Miller H. Neurological diseases in an English city. Acta Neurol Scand 1966;42(suppl 24):9-89 5. Gudmundsson G. Epilepsy in Iceland. A clinical and epidemiological investigation. Acta Neurol Scand 1966;43(suppl 25): 124 p 6. De Graaf AS. Epidemiological aspects of epilepsy in Northern Norway. Epilepsia 1974;15:291-299 7. Gastaut JL. L'epilepsie du vieillard. Perfect Prat 1976;9:63-70 8. Gupta K. Epilepsy in the elderly. How far to investigate. Br J Clin Pract 1983;37:259-262 9. Hauser WA, Kurland LT. The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia 1975;16: 1-66 0. Luhdorf K, Jensen LK, Plesner AM. Epilepsy in the elderly: incidence, social function and disability. Epilepsia 1986;27:135141 1. Luhdorf K, Jensen LK, Plesner AM. Etiology of seizures in the elderly. Epilepsia 1986;27:458-463 la. Loiseau J, Loiseau P, Guyot M, et al. A survey of seizure disorders in the French Southwest: I. Incidence of epileptic syndromes. Epilepsia (in press) 2. Commission on classification and terminology of the International League Against Epilepsy proposal for classification of epilepsies and epileptic syndromes. Epilepsia 1989;30:389-399 3. Hauser WA, Anderson VE, Loewenston RB, McRoberts SM. Seizure recurrence after a first unprovoked seizure. N Engl J Med 1982;307:522-528 4. Cereghino JJ. Epidemiology of epilepsies. Public Health Rev 1974;3:91-100 5. Kurtzke JF. Some epidemiologic and clinical features of adult seizure disorder. J Chron Dis 1968;21:143-156 6. Pond DA, Bidwell BH, Stein L. A survey of epilepsy in fourteen general practices. I. Demographic and medical data. Psychiatr Neurol Neurochir 1960;63:217-236 7. Goodridge DM, Shorvon SD. Epileptic seizures in a population of 6000: I. Demography, diagnosis and classification, and role of the hospital services. Br Med J 1983;287:641-647 8. Juul-Jensen P, Foldspang A. Natural history of epileptic seizures. Epilepsia 1983;24:297-3 12 19. Joensen P. Prevalence, incidence and classification of epilepsy in the Faroes. Acta Neurol Scand 1986;74:150-155 20. Bonduelle M, S d o u C1, Guillard J. Etude de 51 dossiers d'kpilepsie ayant dkbutk apr& 60 ans. Sem Hop Paris 1970;46: 3141-3144 21. Courjon J, Artru F, Zeskov P. A propos des crises d'kpilepsie apparaissant apr& 60 ans observkes en client& de neurologie dans un service de neurochirurgie. Sem Hop Paris 1970;46: 3129-3132 22. Carney LR, Hudgins RL, Espinoza RE, Mass DW. Seizures beginning after the age of 60. Arch Intern Med 1969;124:707709 23. Vercelletto P, Delobel R. Etude des facteurs ktiologiques et
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pronostiques dans les epilepsies debutant aprl.s 60 ans. Sem Hop Paris 1970;46:3133-3137 Schold C, Yarnell PR, Earnest MP. Origin of seizures in the elderly patients. JAMA 1977;238:1177-1178 Hildick-Smith M. Epilepsy in the elderly. Age Ageing 1974;3: 203-208 Woodcock S, Cosgrove JBR Epilepsy after age 50. Neurology 1964;14:34-40 Poirrier R, Franck G, Franc0 G, et al. L'epilepsie inaugurale de I'homme ag6. Rev Med Liege 1982;37:313-322 Feuerstein J, Weber M, Kum D, Rohmer F. Etude statistique des crises epileptiques apparaissanr apr& I'ke de 60 ans. Sem Hop Paris 1970;46:3125-3128 Juul-Jensen P. Epilepsy: a clinical and social analysis of 1020 adult patients with epileptic seizures. Acta Neurol Scand 1964; 4O(suppl 5):148 p De Reuck JL.Neuropathology of epilepsy resulting from cerebrovascular disorders. In: Parsonage M, Grant RHE, Craig AG, et al, eds. Advances in epileptology, XIVth Epilepsy International Symposium. New York Raven Press, 1983:95-98 Richardson EP, Dodge PR. Epilepsy in cerebrovascular disease. Epilepsia 1954;3:49-65 Otomo E. Convulsion in the aged. Folia Psychiatry Neurol Jpn 1981;3:295-299 Luhdorf K, Jensen LK,Plesner AM. Epilepsy in the elderly: life
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Loiseau et al: Seizures in Elderly Patients
237
Loiseau, MD," Pierre Loiseau, MD," Bernard Duchk, MD,' Martine Guyot, MD," Jean-Franfois Dartigues, MD,'? and Bruno Aublet, MDt ~~
An underestimation of epileptic seizures occurring in aged patients is likely. In an epidemiological survey undertaken in Southwest France, the annual incidence rate per 100,OOO persons 60 years or older was 127.2 for all seizures (101.3 in persons aged 60 to 69, 150.4 in those aged 70 to 79, and 139.9 in persons 80 years or older). It was 34.1 for symptomatic localization-related and undetermined epilepsies, 16.1 for isolated seizures, and 77.0 for seizures related to an acute situation, such as metabolic derangements, stroke, or head trauma. In this survey, seizures with an onset age of 60 or older represented 28.0% of the confirmed epilepsies, 17.5% of the isolated seizures, and 52.6% of the acute symptomatic seizures. These figures differ dramatically from those in most previous reports concluding that age-specific incidence declined through adult life. They are closer to the data from more recent reports. The main reason for such a high incidence of epileptic seizures in elderly patients is the number of acute symptomatic (or situation-related) seizures. However, even chronic epilepsies increase in frequency in aging persons. Cerebrovascular disease was the most frequently recognized origin (53.9% of the patients with confirmed epilepsies) and brain tumor was found in 32.9% of the patients. Loiseau J, Loiseau P, Duch6 B, Guyot M, Dartigues J-F, Aublet B. A survey of epileptic disorders in southwest France: seizures in elderly patients. Ann Neurol 1990;27:232-237
Methods
It is generally accepted that about 75% of epilepsies begin before the age of 20 years. This figure, given by Gowers [l} and later by Lennox and Lennox 121, has been confirmed in classic epidemiological surveys. It has been also stated that after age 20 age-specific incidence declines to a rather low level that remains fairly constant throughout adult life or decreases in each subsequent decade of age 13-61. The onset of a seizure disorder in the elderly is held to be rare. In aged patients, nonepileptic fits (i.e., syncopal attacks) are considered much more frequent than epileptic seizures (81% versus 14%, respectively C71). However, in more recent years, the occurrence of epileptic seizures in the elderly has been considered less rare [S]. Agespecific incidence increases in the last decades of life 191 and is more than 100 per 100,000 1101. A large body of literature exists concerning the origins of epileptic seizures in the elderly. Very different figures have been published 1111. The aim of our study was to evaluate the incidence and causes of epileptic seizures in persons 60 years or older.
The present study is part of an epidemiological survey undertaken in Southwest France. The population at risk resided in the department of Gironde, an administrativedistrict around Bordeaux. In a 1982 census there were 1,128,164 residents, 223,224 of whom were 60 years or older. Eligible persons were all those who experienced the first epileptic seizure of their life during the period of March 1, 1984, to February 28, 1985, and who came to medical attention. As the Gironde population increases very slowly, the 1982 census gave a fair estimate of the 1984 population. Data were prospectively collected by all the neurologists and electroencephalographersof the department and bordering towns. Information available from the cards they completed included name, address, date of birth, sex, history of illness, age at onset of symptoms, description of seizures, possible cause, physical and neurological findings, and date and results of electroencephalograms (EEGs) and of computed tomographic (CT) scanning. A retrospective complementary survey was made in the hospital neurology departments. All data were reviewed by us. Further information was obtained by examining medical records and by further questioning patients, family, or patients' physicians during the follow-up
From the "Department of Neurology, University Hospital, Bordeaux, and tDepartment of Epidemiology, University of Bordeaux, Bordeaux, France.
Received Apr 17, 1989, and in revised form Aug 8. Accepted for publication Aug 9, 1989. Address correspondence to Dr Loiseau, Hopital Pellegrin, 33076 Bordeaux, France.
232 Copyright 0 1990 by the American Neurological Association
period. The difficulties and biases of the survey will be discussed in another paper El la]. They are mainly related to the case ascertainment method: Even in Southwest France, which has a very high number of physicians, we are not sure that all patients come to medical attention after a first seizure. An underestimation is even more likely in elderly patients than in children or young adults. Seizures are often poorly described by elderly persons. A classification according to seizure type would be of dubious value. It was easier and more precise to consider epileptic syndromes. An epileptic syndrome is an epileptic disorder characterized by a cluster of signs and symptoms customarily occurring together 1121. According to the proposal for a classification of epilepsies and epileptic syndromes made by the Commission on Classification and Terminology of the International League against Epilepsy [121, four epileptic syndromes are found in aged patients. 1. Symptomatic localization-related epilepsies: Diagnosis is based on any sign or symptom of anatomical localization (i.e., partial seizures or EEG or CT signs of localization). A first subgroup corresponds to remote symptomatic seizures { 131. Seizures occur in patients with a history of central nervous system insult that is thought to be associated with an increased risk of epilepsy when the lapse of time between the insult and the first seizure is more than 1 week. Patients presenting such etiological evidence were considered epileptic even if they had experienced only one seizure at the time of diagnosis. Patients with no known cerebral insult and with no focal abnormalities on CT scan constituted the second subgroup. They were accepted as epileptic only when they had experienced more than one focal seizure at the time of first referral to a specialist. 2. Undetermined epilepsies: This category covers all patients without unequivocal generalized or focal seizures and without etiological factors. Patients had to have experienced more than one seizure at the time of referral. 3. Isolated, apparently unprovoked epileptic events: This category includes patients with isolated seizures, either partial or generalized, without EEG- or CT-detected abnormalities, and without etiological factors. 4. Situation-related seizures: These were named acute symptomatic seizures by Hauser and colleagues [ 131. Others have called them provoked seizures. They are associated with metabolic disorders, alcohol consumption or withdrawal, central nervous system infection, stroke, or head trauma within 7 days of the onset of seizures. They are often but not necessarily isolated epileptic events. Some patients experience several seizures during a unique acute illness. Some patients present with repeated seizures, each related to a recurrent acute situation (i.e., hypoglycemia or alcohol).
The following criteria were used for identification of etiological factors in symptomatic localization-related epilepsies and situation-related seizures:
1. Cerebrovascular disease: either unequivocal evidence of a remote or a recent stroke or subarachnoid hemorrhages, diagnosed either on clinical grounds or CT scanning, or clear evidence of hemodynamic disturbances sufficient for modifying cerebral blood flow. (All patients of the latter group were considered as having had situation-related seizures.) 2. A severe head trauma for remote symptomatic seizures, and any head trauma for acute symptomatic seizures. 3. CT evidence of brain tumor. 4. A documented metabolic disorder with marked electrolyte or glycemic abnormalities. 5. Acute abuse or withdrawal of alcohol in chronic alcoholic patients. 6. Clinical and neuropsychological signs of dementia. 7. Symptoms and signs of meningitis or encephalitis.
Results Two hundred and eighty-four patients were accepted for the study. The annual incidence rate for all seizures (whatever their category) was 127.2 per 100,000 persons 60 years or older. Age-specific and sex-specific incidence rates for all seizures are presented in Table 1. Incidence rates increased with age and were significantly higher for men. Table 2 presents annual incidence rates by type of epileptic syndrome and by sex. Situation-related seizures (i.e., acute symptomatic seizures) were the most frequent. For three of the syndromes, the incidence rate was higher for men. In the present survey, among 804 patients considered as having had a first nonfebrile seizure during the recording period, 284 were 60 years or older. They represent 28.0% of the confirmed epilepsies, 17.5% of the isolated seizures, and 52.6% of the acute symptomatic seizures in the total sample. Table 3 presents annual incidence rates by type of epileptic syndrome and by age groups. Only the incidence for situation-related seizures increased with age. A cause of seizure could be identified in 68 patients with spontaneous seizures (Table 4). By definition, undetermined epilepsy (2 patients) and isolated seizures (36 patients) have no known cause. Cerebrovascular
Table I . Age and Sex-Specifc Annual Incidence Rate of Seizures in Elderly Patients per 100,000 Population Men
Women
Total
Age (yr)
No.
Population
Rate
No.
Population
Rate
No.
Population
Rate
60-69 70-79 80 + Total
65 65 26 156
43,952 33,421 12,876 90,248
147.9 194.5 201.9 172.8
32 60 36 128
5 1,792 49,7 12 31,472 132,976
61.8 120.7 114.4 96.2
97 125 62 284
95,744 83,132 44,348 223,224
101.3 150.4 139.9 127.2
Loiseau et al: Seizures in Elderly Patients
233
Table 2. Sex-SpecificAnnual Incidence Rate of Epileptic Syndromes in Patients Aged 60 or Older per 100,000 Population Men
Symptomatic localization-related epilepsies Undetermined epilepsies Isolated seizures Situation-related seizures
Total
Women
No.
Rate
No.
Rate
No.
Rate
51
56.5 0.0 23.3 93.1
23 2 15 88
17.3 1.5 11.3 66.2
74 2 36 172
33.2 0.9 16.1 77.0
0
21 84
Table 3. Age-SpecificAnnual Incidence Rate of Epileptic Syndromes in Elderb Patients per 100,000 Population Symptom LocalizationRelated Epilepsies
Undetermined Epilepsies
SituationRelated Seizures
Isolated Seizures
Age (Y r)
Population
No.
Rate
No.
Rate
No.
Rate
No.
Rate
60-69 70-79 80 +
95,744 83,132 44,348
34 31 9
35.5 37.3 20.3
1 0 1
1.0 0.0 2.2
14 15 7
14.6 18.0 15.8
48 79 45
50.1 95.0 101.5
disease was the most frequently recognized origin, found in 36.6% of patients with spontaneous seizures and in 53.9% of patients with confirmed epilepsy. Its sex-specific incidence rate was significantly higher in men. Sixty-two (66.7%) of the 93 patients who had seizures within the acute phase of a stroke died-13 within the first week, 17 within the first month, 14 within the first 6 months, 8 within the first year, and 10 within 3 years after stroke. Among our 41 patients with late vascular epilepsy, 30 had ischemic lesions and 3 had sequelae of hematoma. The nature of the lesion was not documented in the other 8 patients. A brain tumor was found in 22.3% of patients with spontaneous seizures, representing a similar percentage of etiological factor in both sexes, but with an incidence 4 times higher in men. Ten patients had glioblastoma and 11 had metastasis. Situation-related seizures (Table 5) had a vascular origin in half of the patients. They were associated with stroke in 56 patients and with cardiac failure in 37 atherotic patients. Toxic seizures were more frequent in number and in incidence in men because they were mainly alcohol related.
Discussion In an epidemiological survey, one of the major difficulties is deciding what to include. Epilepsy is characterized by the occurrence of at least two unprovoked seizures separated by a greater than 24-hour interval. We referred to this as confirmed epilepsy and added to this group a few patients who had experienced only one seizure at the time of referral but who had a high risk of recurrence. Patients who have an accidental or a 234 Annals of Neurology Vol 27 No 3 March 1990
situation-related seizure will not necessarily develop other seizures. Obviously, they are different from those having chronic epilepsy. However, these patients may require specific investigation, treatment, and care E14). Hence, they are important from an epidemiological viewpoint. A nice solution was chosen by Hauser and Kurland 191. They classdied cases of seizures in four categories: (1) recurrent epileptic attacks; (2) single epileptic attack without known cause; (3) single or multiple seizures, each associated with an acute illness; and (4) febrile convulsions. The 1989 proposal for the classification of epileptic syndromes 112) affords another solution, since all patients without recurrent seizures may be included under the heading of special syndromes. When all the seizures (isolated or recurrent unprovoked seizures and situation-related seizures) are considered, an annual incidence rate of 127.2 per 100,000 persons aged 60 years or older differs dramatically from the rates of other studies 115-171. In one instance it was found to be 33 per 100,000 fl81. However, Luhdorf and colleagues {lo) in Denmark retrospectively studied the incidence of epileptic seizures in persons who were older than 60 years and who were admitted to a hospital that received virtually all patients from the region. They assumed that practically all the elderly with fits were diagnosed. The incidence rate and age curve for patients presenting with a first seizure during the study period were very similar to ours: The mean annual incidence rate per 100,000 at 60 years or older was 104; incidence rates in the age ranges 60 to 64, 65 to 69, 70 to 74, 75 to 79, and 80 and older were 79, 111, 131, 123, and 76, respec-
Table 4. Cause of Symptomatic Localization-Related Epilepsies in 284 Patients with First Seizure at Age 60 or Older
Men Origin
No.
Incidence Rate
Vascular Tumor Traumatic Unknown Total
27 18 1
29.9 19.9 1.1
5
5.5
51
56.5
Women
Total
%
No.
Incidence Rate
%
No.
Rate
%
52.9 35.3 2.0 9.8 100
14 7 1 1 23
10.5 5.3 0.8 0.8 17.3
60.9 30.4 4.3 4.3 100
41 25 2 6 74
18.4 11.2 0.9 2.7 33.2
55.4 33.8 2.7 8.1 100
Incidence
Table 5 . Cause of Situation-Related Seizures in 284 Patients with First Seizure at Age 60 or Older
Men Origin
No.
Vascular Metabolic Toxic Dementia Traumatic Infection Total
42 12 18 4
6 2 84
Women
Total
Incidence
Incidence Rate
%
No.
Rate
46.5 13.3 19.9 4.4 6.6 2.2 93.1
50.0 14.3 21.4 4.8 7.1 2.4 100
51 14 7 12 1 3
38.4 10.5 5.3 9.0 0.7 2.2 66.2
88
tively. They included all first seizures, either spontaneous or provoked. When only definite cases of epilepsy were considered, the incidence rate was 77 per year per 100,000 persons at age 60 or older. Concerning the age- and sex-specific incidences of the various epileptic syndromes in patients 60 years or older (see Table 2), some comments may be made. First of all, the main reason for so high an incidence of epileptic seizures in elderly patients was the number of acute symptomatic seizures. Secondly, the situationrelated seizure rate increased dramatically after the age of 70 (see Table 3). The rate for confirmed epilepsy was much higher in men than in women, whereas the rate of acute symptomatic seizures was not very different between sexes. Isolated seizures occupied an intermediate position. As for confirmed epilepsy, our figure is once more very different from previously reported ones. Annual incidence rate for confirmed epilepsy in persons aged 60 or older was found to be 6.2 per 100,000 151 or 15 per 100,000 1191, 15.7 per 100,000 for persons aged 60 to 69 and 7.6 per 100,000 for 70 or older 141, and 17 per 100,000 for persons aged 60 to 69 and 12 per 100,000 for 70 or older C61. However, our data are less impressive than that of Hauser and Kurland [91, who reported an incidence rate of 82.0 per 100,000 in patients older than 60 during the period 1965 to 1967. This is probably due to a longer follow-up period at the Mayo Clinic, with recurrence of seizures over time. However, their incidence of
% 58.0 15.9 8.0 13.6 1.1 3.4 100
No.
Incidence Rate
%
93 26 25 16 7 5 172
41.7 11.6 11.2 7.2 3.1 2.2 77.0
54.1 15.1 14.5 9.3 4.1 2.9 100
isolated spontaneous or provoked convulsive disorders (69.4/100,000 131) was lower than ours, but the authors expected a marked underestimation in this category due to their case-record system. Vascular disease is generally considered a prominent cause of seizures in the elderly. However, its etiological position has been diversely estimated: 4% 1201, 17% 1211, 18% 1221, 26% 1231, 28% 1241, 32% 1111, 42% 1251, 43% 126, 271, 50% C81, 52% 1281, and 69.2% r29). The problem arises from the various meanings given to the term vascakzr disease. Either in the acute phase of a cerebral infarct or intracranial bleeding or long after it, postapoplectic seizures are a well-defined entity. Only these seizures were taken into account by some [ l l , 241. But other authors assumed that nonspecific extracerebral atherosclerosis may cause epilepsy on the assumption that systemic vascular disease is associated with cerebrovascular disease. This assumption has been considered rather speculative 1113. However, De Reuck 1301 expressed doubts as to whether vascular epilepsy can be the result of the presence of a cerebral infarct alone and stressed the importance of additional exogenous factors, such as hypertensive episodes, periods of cardiac failure, or respiratory or metabolic disorders. For this reason, we distinguished two forms of seizures of acute vascular origin: clearly postapoplectic seizures and seizures occurring during severe hemodynamic disturbances. Seizures at the onset of stroke have a practical Loiseau et al: Seizures in Elderly Patients 235
interest. It is widely held that patients who have seizures within the acute phase of a stroke have a poor prognosis 131-34). The proportion of epileptogenic brain tumors in elderly patients differs widely between studies, ranging from 2 to 28% (see {ll))according to the source of data (neurosurgeons, neurologists, electroencephalographers, internists, inpatients or outpatients, and so on) and to the inclusion criteria (absence or presence of neurological symptoms other than epilepsy). Most of the tumors found in elderly patients were malignant 111, 22). In some studies cerebral atrophy shown by CT has been considered an etiological factor 111, 351. We share the opinion expressed by Shorvon and colleagues 136): It is quite common in elderly persons, without any correlation with neurological status. It cannot be considered a causative factor in epileptic disorders. The proportion of patients with an unknown cause differs according to whether all spontaneous seizures (n = 112) or confirmed epilepsy only (n = 76) are considered (39.3% versus 10.596, respectively). A follow-up period with recurrence of isolated cryptogenic seizures would modify these figures. The published data for epilepsies with an onset in patients older than 50 in whom no etiological factor is found are 50% 121, 241, 28% E81, 25% 1111, 22% 1371, or 16% 138). The introduction of CT scanning and magnetic resonance imaging lowered the percentage of late-onset epilepsy with unknown cause. Unsuspected cerebral infarcts can provoke seizures with no recognizable stroke 136, 38-41). Situation-related seizures need no further comment except on their frequency. Because an important effort was made to detect them, they are more numerous in this study than in series reported from neurological centers. The underlying illness is the dominant clinical feature. It is easily recognized and the patient is not referred for further investigation. Some seizures probably escape medical attention. Seizures in demented patients are not rare 18, 25, 383 but are often single events in patients with metabolic derangements. For this reason, they were included in the group of situation-related seizures. This study was supported in part by Sanofi, Synthelabo, and the Direction Rkgionale des Affaires Sanitaires et Sociales of Aquitaine. We thank Drs M. Aupy, A. Banayan, CI. Bensch, D. Bequet, A. Biolsi, J. Bourdot, F. Bretegnier, P. Chavois, S. Cohadon, D. Daynes, F. X. Debelleix, M. M. Deliac, F. Dutertre, A. Fournier, J. P. Girard, T. Herbelleau, M. Jogeix, A. Laporte, J. L. Larrieu, M. Legroux, F. Maupetit, J. Paty, M. Pestre, V. Riemens, J. Rozier, J. Saintarailles,E. Sauvan-Vian, F. Terraz, C1. Villeneuve-Bugat, and J. D. Vincent for their kind assistance in collecting data. We are grateful to P. L. Morselli, MD (LERS-Synthelabo), A. Perret, MD (Sanofi), and G. Venaud, M D (Labaz, France), for their help.
236 Annals of Neurology Vol 27 No 3 March 1990
We would also like to thank the doctors in public and private practice who were willing to participate in this survey. We wish to acknowledge Dominique Nicolini for typing and Jim Sneed for assisting in preparation of the manuscript.
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