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Neurological Sciences

, Volume 34, Issue 8, pp 1441–1446 | Cite as

Seizures and epilepsy in elderly patients of an urban area of Iran: clinical manifestation, differential diagnosis, etiology, and epilepsy subtypes

  • Sayed Shahaboddin Tabatabaei
  • Ahmad Delbari
  • Reza Salman-Roghani
  • Leili Shahgholi
  • Reza Fadayevatan
  • Naghmeh Mokhber
  • Johan Lokk
Original Article

Abstract

The incidences of seizures and epilepsy in the population show a peak after 60 years of age. Due to the lack of reported clinical aspects of seizure and epilepsy in the older patients in our region in Iran, this study was conducted to describe the clinical manifestation, etiology, differential diagnosis, and epilepsy subtypes of epilepsy and seizure. A cross-sectional retrospective study was performed on all consecutively elderly seizure and epilepsy patients, referred to the Epilepsy Association in the city of Qom, Iran over a 10-year period. A total of 466 patients aged >60 years were admitted. 31 % of the patients had epilepsy or seizure and 69 % of them had non-epileptic events. The most prevalent differential diagnoses in the beginning were syncope and cardiovascular disorders. The most frequent clinical symptom of epilepsy was generalized tonic–clonic seizures (75 %). The most common cause of seizure was systemic metabolic disorder (27 %). In epileptic elderly patients, no cause was ascertained for 38 % and the most frequently observed pathological factors were cerebrovascular diseases, which accounted for 24 %. The most common type of epileptic seizure was generalized epileptic seizures (75 %). 10 % of elderly epileptic patients suffered from status epilepticus, which was primarily caused by anoxia. Despite the rising rate and potentially profound physical and psychosocial effects of seizures and epilepsy, these disorders have received surprisingly little research focus and attention in Iran. Referring older patients to a specialist or a specialist epilepsy center allows speedy assessment, appropriate investigation and treatment, and less likely to miss the diagnosis.

Keywords

Clinical aspects Elderly Epilepsy Iran Seizure 

Introduction

Acute onset seizures and epilepsy are the two most common neurologic afflictions of the elderly population [1]. Worldwide, the prevalence of epilepsy is estimated to be 50 million cases (0.75 % of world population), and 85 % of these cases originate from the developed countries [2]. Among all the developed countries, the incidence of these conditions is greatest in the population older than 60 years and is estimated to be 134 per 100,000 for epilepsy and 100 per 110,000 for acute onset seizures [3]. In the Iran population, the prevalence of epilepsy is reported to be as high as 1.8 %, yet the epidemiologic data for the elderly population within Iran are limited [4].

Cerebrovascular disease (CVD) is considered to be the primary etiology of epilepsy and acute onset seizures in the elderly [5, 6]. When comparing individuals of similar age and gender, individuals with CVD have a 20-fold increased risk of epilepsy during their lifetime [7]. Unfortunately, as the elderly may not present with typical pre-, peri-, or post-ictal symptoms, the diagnosis of seizure and/or epilepsy may be delayed in this demographic section [1]. As seizure and new-onset epilepsy can be dangerous and even life-threatening in the elderly population, early detection and diagnosis is crucial for the safety of the patient and the population. As there remains a paucity of data regarding the clinical manifestations of seizure and epilepsy in the elderly population, we sought to better define and describe the manifestations, etiologies, differential diagnoses, and subtypes of epilepsy and seizures to facilitate faster and more frequent detection by primary care providers.

Materials and methods

Study design and population

This study was carried out following the approval of the Qom University of Medical Sciences and Epilepsy Association Ethics Committees under the guidelines put forth by the Declaration of Helsinki. All inhabitants of the capital city Qom, Iran older than 60 years, who were diagnosed with epilepsy as defined by WHO criteria [8] between March 1998 and March 2007 were included in this cross-sectional retrospective study. Study participants were identified via retrospective chart review of all diagnoses notes in medical and discharge summaries generated between March 1998 and March 2007 at the Neurology Clinics and Wards of Qom Hospitals. Exclusion criteria included, (1) all patients diagnosed with pseudoseizures and psychogenic events, and (2) neurologic manifestations of CVD, systemic metabolic disorders, psychiatric disorders (e.g., severe anxiety, depression and psychotic symptoms), cortical dysfunction symptoms, musculoskeletal disorders, and balance disorders that shared symptoms common with epilepsy.

Clinical diagnostic criteria

The diagnosis of epilepsy was defined using WHO criteria by an experienced neurologist upon referral by an outside provider to the Epilepsy Association in the city of Qom, Iran. Briefly, the WHO criteria for epilepsy diagnosis include clinical criteria (list these) in addition to EEG, CT, and/or MRI findings consistent with the clinical findings of seizure and epilepsy. All patients received an EEG and CT or MRI of the brain. All patients were required to complete a questionnaire to characterize their seizures to better characterize the demographics, clinical correlations, clinical manifestations, causes, differential diagnosis, and subtypes, of seizure and epilepsy in the elderly population. All physicians and nurses involved in this study received special training with respect to this study.

Clinical definitions

Acute symptomatic seizures

Acute symptomatic seizures are events, whether toxic, metabolic, infectious, structural, or due to inflammation, which happen near in time to acute CVD insult [9].

Epilepsy

Epilepsy or unprovoked seizures are those that occur without a clinical condition being responsible or further removed in time than can be attributed to acute symptomatic seizures. Classification of seizures was in accordance with the guidelines of the International League Against Epilepsy [9].

Non-epileptic events are clinical occurrences that appear similar to epileptic seizures, but are not connected with abnormal cortical electrical discharges [10].

Status epilepticus (SE)

In the older epidemiological studies SE is most commonly defined as more than 30 min of continuous seizure activity, or of intermittent seizures without fully recovering consciousness between seizures [11].

Statistical methods

Variables were described using standard descriptive statistics. Categorical variables were summarized into counts and percentages. Statistical analysis was done with the SPSS 14 software package.

Results

Study population

From March 1998 to March 2007, 466 patients in the Qom province of Iran, representing 0.6 % (466/79.552) of the population above 60 years of age, were admitted for symptoms consistent with seizure and/or epilepsy. Of this study population, 321 (69 %) were eventually excluded from study due to diagnoses of non-epileptic events. The remaining 145 (31 %) patients, 75 men (52 %) and 70 women (48 %) had epileptic and non-epileptic seizure, 100 patients were diagnosed with epilepsy and 45 patients had definitive clinical evidence of an isolated non-epileptic seizure.

Clinical manifestations and etiologies of non-epileptic events

Among excluded individuals, the most common etiologies of pseudoseizures events included cardiogenic syncope as a result of underlying cardiovascular disease (38 %), falls (10.3 %), mental and cognitive disturbances (10 %), psychiatric disorders (panic attacks, depression, conversion reaction) (9.6 %), systemic, metabolic, and infectious diseases (7.2 %), vertigo, transient ischemic attack and transient global amnesia (12.5 %), and unknown (12.5 %).

Clinical manifestations and etiologies of epileptic events

The most common clinical presentations and etiologies of individuals greater than 60 years diagnosed with epilepsy are shown in Tables 1 and 2, respectively. Among 145 of the elderly patients with acute seizure, the most common clinical presentation in this demographic section was generalized tonic–clonic seizures (75 %). In this same subset, the most common cause of seizure was systemic metabolic disorders (27 %, Table 2). The most frequent metabolic derangements associated with seizure included hypoglycemia (33.3 %), hyperglycemia (30.8 %), uremia (28.2 %), hypocalcemia (5.1 %), and hyponatremia (2.6 %). Among individuals diagnosed with seizure, CVD was the most frequent attributable cause (24 %). No obvious etiology could be ascertained in 26 % of individuals with acute seizure and in 38 % of individuals with epilepsy.
Table 1

Clinical symptoms of epilepsy in elderly people

Symptoms

%

Generalized tonic–clonic seizures

75

Focal tonic–clonic seizures

36

Impaired alertness

13

Impairment of consciousness

9

Automatisms

6

Myoclonus

5

Transient amnesia

2

Transient hallucination

2

Some patients had more than one symptom

Table 2

Common cause of epilepsy and acute seizure in elderly patients

Etiology

Acute seizure (%)

Epilepsy (%)

Systemic metabolic disorders

27

 

Idiopathic and cryptogenic

38

55

Cerebrovascular diseases

17

24

Neoplasm

6

8

Anoxia-hypoxia

6

8

Drug-induced

2

 

Trauma

1

2

Degenerative disease

1

2

Acute cerebral infection

1

1

Alcohol

1

 

Total

100

100

It has earlier been found that there is no obvious etiology for 25–45 % of patients who develop epilepsy after the age of 60, even as imaging techniques become more sophisticated [12].

Epileptic seizure classification, causes, and outcomes

Among the 100 individuals who were diagnosed with epilepsy, the most common types of epileptic seizure from most to least common, some patients had more than one type, were generalized epileptic seizures (75 %), mixed seizures (30 %), complex partial seizures (23 %), simple partial seizure (13 %), and myoclonic seizures (5 %). This study found that of 100 cases with epilepsy, 27 % had primary and 24 % secondary tonic–clonic seizures.

Ten percent (10 %) of elderly epileptic patients suffered from SE which, in the majority of cases, was attributed to anoxia (c.f. Table 3). The incidence of generalized tonic–clonic seizures and non-convulsive seizure in patients with SE were 90 and 10 %, respectively. The overall mortality in hospital of these patients presenting with SE was 60 %.
Table 3

Characteristics of status epilepticus

Etiology

Symptoms

N

Outcome

Anoxic brain injury following cardiopulmonary arrest

Generalized tonic–clonic seizures

6

5 patients died, 1 patient continued of treatment with AED

Cerebrovascular disease

Generalized tonic–clonic seizures

3

Continued of treatment with AED

Unknown

Non-convulsive SE (continuous delirium)

1

Continued of treatment with AED

Discussion

The current study demonstrates that clinical aspects of seizures and epilepsy in elderly patients in an urban area of Iran have some differences compared to developed countries. We will discuss these findings in detail below.

Etiology

Unlike younger individuals between the ages of 35–64 years where the most common cause of acute symptomatic seizures is drug withdrawal, systemic metabolic disorders represent the most common identifiable cause of acute symptomatic seizure in the elderly [13]. Compared to the published work of Waterhouse and Towne [1] our findings suggest that metabolic derangement may be a more common cause of seizure in the elderly than stroke, particularly within the Iranian population. Further, our findings may suggest that the Iranian population may differ from the US population [14], as they found that CVD was the most common etiology associated with elderly seizure. In agreement with previous studies, hypoglycemia secondary to excessive insulin use and non-ketotic acidosis was the most common metabolic cause of seizures [15, 16]. Finally, our study found that only 2 % of seizure cases were associated with substance abuse or pharmacologic misadventures. When compared to other studies [17], this rate is roughly five times less than general population and may be a result of cultural differences between Iranian and British society.

Our findings suggest that CVD is the most common cause of epilepsy in the elderly Iranian population, and this is consistent with other reports in the medical literature of both Iranian and non-Iranians. In one recent study of the northern Iranian region, 17.3 % of patients presenting with acute stroke developed at least one seizure within two years of their stroke [18]. Such findings suggest that measures should be undertaken to reduce the rate of CVD through lifestyle modification and early preventative measures to control hypertension and hyperlipidemia.

Clinical manifestations and diagnosis

Significant differences in the clinical manifestations of seizure exist between younger and older patients and are postulated to be a major cause of delayed diagnosis. Since tonic–clonic seizures are uncommon [19], elderly patients may present with atypical symptoms, even though 75 % of patients exhibited generalized tonic–clonic seizures, making it the most common clinical symptom. It might be related to the inclusion of more patients with classic symptoms, or because relatively few of the practitioners in our region are well-educated on epilepsy in the elderly, which can cause misdiagnosis and delayed treatment. Spitz et al. [20] reported that correct diagnosis is frequently delayed in the elderly, mainly because of lack of awareness of partial seizures by the public and healthcare providers and the concept of trying to attribute all of the patients’ symptoms to a single diagnosis. 30 % of the time or more, people are unaware of their seizures [21] and only go to hospital when classic symptoms are manifested.

The reason seizures manifest differently in older patients than in younger, is because of the anterior frontal cortical areas of the brain affected in stroke patients [11]. Over 20 % of patients suffered from impaired consciousness and impaired alertness, which is significantly different from those in younger patients. Ramsay and Pryor [22] reported that often patients describe seizures as altered mentation, periods of staring, unresponsiveness, or blackout spells in the elderly. These factors make it more difficult to diagnose epilepsy correctly in elderly patients.

Differential diagnosis

Epilepsy is often misdiagnosed in younger patients and even more commonly in the elderly. Our study found that the majority of elderly patients with seizure or epilepsy were initially misdiagnosed, and this finding is consistent with previous reports. Ramsay et al. [23] reported that alternative diagnoses were altered mental status (41.8 %), confusion (37.5 %), blackout spells (29.3 %), memory disturbance (17.2 %), syncope (16.8 %), dizziness (10.3 %), and dementia (6.9 %). The particular challenges of differential diagnosis in elderly patients demand special attention. The diagnosis of epilepsy in elderly patients is limited by four factors: (1) many patients cannot produce an exact history of their seizures, and are often difficult to observe; (2) the epilepsy is often misdiagnosed because of insufficient epileptic knowledge from primary care providers; (3) cognitively impaired elderly individuals are often unwilling or unable to cooperate during examinations, and (4) diagnosis is limited by the cognitive compromise as a result of neurological or psychiatric comorbidities in the elderly [24].

Epileptic seizure types

Our study showed that the most common epileptic seizure type for older patients in our region was generalized epileptic seizure, in disagreement with previous reports that implicate complex partial seizures as the most common cause [19]. The reasons for this incongruent finding are unclear, but may be a result of a lack of video-EEG monitoring in the city of Qom, as paroxysmal events often require video-EEG monitoring [1]. In contrast, generalized tonic–clonic seizures are easier to identify in the absence of video-EEG monitoring.

Status epilepticus

Our results showed that SE was much more common than has been reported in the medical literature. SE is estimated to occur in between 1.3 and 12.3 % of adult epileptic patients [3]. SE was probably more common in our study partly, because our patient population was biased towards individuals who were admitted with symptomatic seizures. Consistent with other reports, anoxia was the most common cause of SE in older patients. However, Wu et al. [25] showed that the prevalent etiology of SE was a delayed effect of brain injury or stroke, in older Californian patients.

In older patients, the etiology of SE is one of the major determinants of mortality, in addition to patient age and duration of SE [26]. Our SE patients had a mortality rate of about 60 %, which is higher than the previous studies in adults, which vary from 2.5 % to about 20 % [27]. The highest mortality was found in SE patients with anoxia, with a mortality rate of about 84 %, which is in agreement with the earlier studies [26].

Several limitations exist in our study. First, our study was not strictly population-based, even though it was the first study of this type in an urban area of Iran. Cases were found by screening medical records, and this presumably excludes some patients who had not been admitted to a hospital or clinic. Second, the accuracy of our findings is complicated by the fact that older people are more prone to live alone and are thus, less reliable regarding medical history. Finally, video-EEG monitoring was not available to us, and may thus, limit our ability to classify seizure types in older patients.

Conclusions

Seizures and epilepsy in the elderly are two most common neurologic problems with considerable pathologic, psychosocial, and economic burden on society. Despite the rising rate of elderly persons and potentially profound physical and psychosocial effects of seizures and epilepsy, these disorders have received surprisingly little research focus and attention in Iran. Referring older patients to a specialist or a specialist epilepsy center allows for more expeditious assessment, investigation, and accurate diagnosis.

References

  1. 1.
    Waterhouse E, Towne A (2005) Seizures in the elderly: nuances in presentation and treatment. Clevel Clin J Med 72(Suppl 3):S26–S37CrossRefGoogle Scholar
  2. 2.
    Press A (2011) Ignorance is not bliss: epilepsy in third world countries. http://www.epilepsyontario.org/client/EO/EOWeb.nsf/web/Epilepsy+in+Third+World+Countries. Accessed 16 June 2011
  3. 3.
    Thomas RJ (1997) Seizures and epilepsy in the elderly. Arch Intern Med 157(6):605–617PubMedCrossRefGoogle Scholar
  4. 4.
    Mohammadi MR, Ghanizadeh A, Davidian H, Mohammadi M, Norouzian M (2006) Prevalence of epilepsy and comorbidity of psychiatric disorders in Iran. Seizure 15(7):476–482PubMedCrossRefGoogle Scholar
  5. 5.
    Hauser WA (1997) Epidemiology of seizures and epilepsy in the elderly: seizures and epilepsy in the elderly. Butterworth-Heinemann, Boston, pp 7–18Google Scholar
  6. 6.
    Paradowski B, Zagrajek MM (2005) Epilepsy in middle-aged and elderly people: a three-year observation. Epileptic Disord 7(2):91–95Google Scholar
  7. 7.
    Hauser WA, Ramirez-Lassepas M, Rosenstein R (1984) Risk for seizures and epilepsy following cerebrovascular insults [abstract]. Epilepsia 25:666Google Scholar
  8. 8.
    World Health Organization. Available from: http://www.who.int/topics/epilepsy/en/. Accessed 16 June 2011
  9. 9.
    Beghi E, Carpio A, Forsgren L, Hesdorffer DC, Malmgren K, Sander JW et al (2010) Recommendation for a definition of acute symptomatic seizure. Epilepsia 51(4):671–675PubMedCrossRefGoogle Scholar
  10. 10.
    Patel H, Dunn DW, Austin JK, Doss JL, LaFrance WC Jr, Plioplys S et al (2011) Psychogenic nonepileptic seizures (pseudoseizures). Pediatr Rev 32(6):e66–e72PubMedCrossRefGoogle Scholar
  11. 11.
    Waterhouse EJ (2001) Status epilepticus in older patients: epidemiology and treatment options. Drugs Aging 18(2):133–142PubMedCrossRefGoogle Scholar
  12. 12.
    Hauser WA, Annegers JF, Kurland LT (1993) Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935–1984. Epilepsia 34(3):453–458PubMedCrossRefGoogle Scholar
  13. 13.
    Annegers J, Hauser W, Lee J (1995) Incidence of acute symptomatic seizures in Rochester, Minnesota, 1935–1984. Epilepsia 36(4):327–333PubMedCrossRefGoogle Scholar
  14. 14.
    Sirven JI (2001) Acute and chronic seizures in patients older than 60 years. Mayo Clinic Proc 76(2):175–183Google Scholar
  15. 15.
    Malouf R, Brust J (1985) Hypoglycemia: causes, neurological manifestations, and outcome. Ann Neurol 17(5):421–430PubMedCrossRefGoogle Scholar
  16. 16.
    Singh BM, Strobos RJ (1980) Epilepsia partialis continua associated with nonketotic hyperglycemia: clinical and biochemical profile of 21 patients. Ann Neurol 8(2):155–160PubMedCrossRefGoogle Scholar
  17. 17.
    Franson K, Hay D, Neppe V, Dahdal W, Mirza W, Grossberg G et al (1995) Drug-induced seizures in the elderly. Causative agents and optimal management. Drugs Aging 7(1):38–48PubMedCrossRefGoogle Scholar
  18. 18.
    Nikanfar M, Arami M, Najmi LMS (2005) Common etiologies of adult onset epilepsies in northwest of Iran. Acta Medica Iranica 43(3):223–226Google Scholar
  19. 19.
    Cloyd J, Hauser W, Towne A, Ramsay R, Mattson R, Gilliam F et al (2006) Epidemiological and medical aspects of epilepsy in the elderly. Epilepsy Res 68:39–48CrossRefGoogle Scholar
  20. 20.
    SpitzMC BJ, Ramsay ER et al (2000) Observations on the delay in the diagnosis of seizures in the elderly [abstract]. Epilepsia 41(7):109Google Scholar
  21. 21.
    Van Cott AC (2002) Epilepsy and EEG in the elderly. Epilepsia 43:94–102PubMedCrossRefGoogle Scholar
  22. 22.
    Ramsay RE, Pryor F (2000) Epilepsy in the elderly. Neurology 55(5 Suppl 1):S9–S14PubMedGoogle Scholar
  23. 23.
    Ramsay RE, Rowan AJ, Pryor FM (2004) Special considerations in treating the elderly patient with epilepsy. Neurology 62(5 suppl 2):S24–S29PubMedCrossRefGoogle Scholar
  24. 24.
    Stefan H (2011) Epilepsy in the elderly: facts and challenges. Acta Neurol Scand 124(4):223–237PubMedCrossRefGoogle Scholar
  25. 25.
    Wu Y, Shek D, Garcia P, Zhao S, Johnston S (2002) Incidence and mortality of generalized convulsive status epilepticus in California. Neurology 58(7):1070–1076PubMedCrossRefGoogle Scholar
  26. 26.
    Towne AR, Pellock JM, Ko D, DeLorenzo RJ (1994) Determinants of mortality in status epilepticus. Epilepsia 35(1):27–34PubMedCrossRefGoogle Scholar
  27. 27.
    Towne AR (2007) Epidemiology and outcomes of status epilepticus in the elderly. Int Rev Neurobiol 81:111–127PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2012

Authors and Affiliations

  • Sayed Shahaboddin Tabatabaei
    • 1
  • Ahmad Delbari
    • 2
    • 3
  • Reza Salman-Roghani
    • 1
  • Leili Shahgholi
    • 4
  • Reza Fadayevatan
    • 1
  • Naghmeh Mokhber
    • 5
  • Johan Lokk
    • 2
  1. 1.Iranian Research Center on AgingUniversity of Social Welfare and RehabilitationTehranIran
  2. 2.Division of Clinical Geriatrics, Department of Neurobiology, Care Sciences and Society, R94, Karolinska InstituteHuddinge HospitalStockholmSweden
  3. 3.Iranian Research Center on Healthy AgingSabzevar University of Medical SciencesSabzevarIran
  4. 4.Physical Medicine and Rehabilitation DepartmentMayo ClinicRochesterUSA
  5. 5.Psychiatry and Behavioral Sciences Research CenterMashhad University of Medical ScienceMashhadIran

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