Ratios of Nine Risk Factors in Children With

Recurrent Febrile SeizuresAyse Tosun, MD*, Guldane Koturoglu, MD†, Gul Serdaroglu, MD†, Muzaffer Polat, MD‡,

Zafer Kurugol, MD†, Sarenur Gokben, MD†, and Hasan Tekgul, MD†

Febrile seizures are the most common convulsive disorderof childhood, with a recurrence probability of 33%. Theaim of the study was to determine the risk factors for re-currence of febrile seizures in children. In this descriptive,cross-sectional study, nine risk factors of recurrence offebrile seizures were investigated in 259 children withfebrile seizures: (1) sex; (2) domicile; (3) income level;(4) family history of febrile seizures; (5) family historyof epilepsy; (6) level of fever; (7) duration of fever; (8)type of seizure, simple vs complex; and (9) age at seizureonset. The risk factors were compared for 119 childrenwith isolated febrile seizures (45.9% of the total) and140 children with two or more febrile seizure recurrences(54.1%). Among the patients with and without recurrentfebrile seizures, 32% and 18% were domiciled in nonur-ban areas, respectively (P = 0.012). There was a family his-tory of febrile seizures in 57% and 44% of cases with andwithout recurrent febrile seizures, respectively (P =0.031). According to the logistic regression analysis, a fam-ily history of febrile seizures was a risk factor that affectedrecurrence (P = 0.018; odds ratio OR = 1.933; 95% confi-dence interval CI = 1.121-3.333). We also found that domi-cile (P = 0.001) and income (P = 0.013) were risk factorsfor recurrence. A family history of epilepsy was not a sig-nificant risk factor (P = 0.129; OR = 2.110; 95% CI =0.804-5.539). � 2010 by Elsevier Inc. All rights reserved.

Tosun A, Koturoglu G, Serdaroglu G, Polat M, Kurugol Z,

Gokben S, Tekgul H. Ratios of nine risk factors in children

with recurrent febrile seizures. Pediatr Neurol 2010;43:177-

182.

Introduction

Epidemiologic studies have demonstrated the importance

of environmental and personal factors, particularly genetic

From the *Department of Pediatrics, Adnan Menderes University MedicalFaculty, Aydin, Turkey; the †Department of Pediatrics, Ege UniversityMedical Faculty, Izmir, Turkey; and the ‡Department of Pediatrics, CelalBayar University Medical Faculty, Manisa, Turkey.

� 2010 by Elsevier Inc. All rights reserved.doi:10.1016/j.pediatrneurol.2010.05.007 � 0887-8994/$—see front matter

factors, in the development of first febrile seizures in chil-

dren, as well as recurrent febrile convulsions [1-8].

Although febrile seizures are generally benign, they

remain important, based on the risk of developing

epilepsy (a relatively low risk) but especially on risk of

recurrence, seen in 23-42% of cases [1,5,9-11].

The decision to initiate prophylaxis and determining the

prognosis of febrile seizures are important issues for the

clinician. A family history of febrile seizures, early age at

onset, lower temperature at the time of febrile seizures,

and shorter duration of fever before the febrile seizures

are the significant risk factors for recurrent febrile seizures

[1,9,10,12,13]. Although a family history of epilepsy,

seizures with complex features, and neurodevelopmental

abnormality are known risk factors for developing

epilepsy, their status as risk factors for recurrent febrile

seizures remains controversial [1,4,8,10,13,14].

For two of the generally accepted risk factors for

recurrent febrile seizures (i.e., for the level of fever required

to diagnose febrile seizure and for the duration of fever

prior to the seizure), different definitions have been

used in different studies [1,7,9,10,12]. The objective of

the present study was to determine the ratios of nine

generally accepted risk factors for recurrent febrile

seizures in a sample of children with and without

recurrent febrile seizures.

Methods and Patients

Risk Factors, Study Population, and Methods

The study was designed to address nine generally accepted risk factors

for recurrent febrile seizures: (1) sex; (2) domicile of family, urban vs non-

urban; (3) income level of family, relative to subsistence; (4) family history

of febrile seizures; (5) family history of epilepsy; (6) level of fever causing

seizures, (7) duration of fever before seizures, (8) type of seizure, simple vs

complex; and (9) age at seizure onset.

Communications should be addressed to:Dr. Koturoglu; Department of Pediatrics; Ege University Medical School;35040 Bornova-Izmir, Turkey.E-mail: guldane.koturoglu@ege.edu.trReceived December 31, 2009; accepted May 3, 2010.

Tosun et al: Risk Factors in Febrile Seizures 177

Table 1. Risk factors in 259 febrile seizure patients with (Positive)

and without (Negative) recurrence

Patients, no. (%)*Risk Factors Negative Positive P value

Sample size n = 119 n = 140

Sex

Male 67 (56) 80 (57) 0.892

Female 52 (44) 60 (43)

Domicile

Urban 97 (82) 95 (68) 0.012

Nonurban 22 (18) 45 (32)

Income level

# Subsistence wage 26 (22) 13 (9) 0.005

> Subsistence wage 93 (78) 127 (91)

Family history of febrile seizure

Positive 52 (44) 80 (57) 0.031

Negative 67 (56) 60 (43)

Family history of epilepsy

Positive 7 (6) 20 (14) 0.027

Negative 112 (94) 120 (86)

Level of fever

#39�C 69 (58) 75 (54) 0.747

>39�C 50 (42) 59 (42)

Duration of fever before seizure

#1 hour 38 (32) 28 (20) 0.046

>1 hour 81 (68) 106 (79)

Complex febrile seizure

Positive 16 (13) 17 (12) 0.754

Negative 103 (87) 123 (88)

Age at seizure onset

#18 months 61 (51) 87 (62) 0.078

Included in the present study were 259 children admitted to the Ege

University Medical School Department of Pediatrics, Division of Child

Neurology, and the Emergency Department between January 2004 and

January 2008 with a history of a febrile seizure and normal findings on

neurologic examination. Children with seizures during fever with an

axillary temperature of 37.8�C or higher were categorized as febrile seizure

patients [12,15].

Children who had their first febrile seizure between 3 months and 5

years of age and who presented with recurrent seizures after the age of 5

years were eligible for inclusion. Excluded from the study were children

who had evidence of intracranial infections or head trauma, history of neo-

natal seizures, afebrile seizures, developmental retardation, or pathologic

findings on the neurologic examination prior to admission.

Level of fever was recorded as axillary temperature measured by the

medical staff at admission to the emergency department during the time

of the febrile seizure, or axillary temperature measured by the family prior

to admission. An axillary temperature of 39�C or less was defined as low

fever.

The following sociodemographic characteristics and clinical data were

recorded on previously designed forms: domicile (urban vs nonurban), pa-

rental education (primary school vs lower-secondary school or higher),

family income (relative to the subsistence wage level, defined as 500

Turkish liras), type of family (nuclear vs extended), family history of con-

sanguinity, family history of febrile seizures, family history of epilepsy,

level of fever during the seizure (#39�C vs >39�C), seizure duration

(#15 minutes vs >15 minutes), type of seizure (generalized tonic-clonic,

focal, or atonic), classification of the seizure (complex [i.e., focal, pro-

longed than 15 minutes, and recurrences in 24 hours or within the same fe-

brile illness] vs simple), time from onset of fever to seizure (#1 hour vs >1

hour, or #24 hours vs <24 hours), cause of fever (upper respiratory tract

infection, lower genital tract infection, urinary tract infection, or postvacci-

nation), total number of febrile seizures at admission, and the history and

reason for any hospitalization in the neonatal unit.

>18 months 58 (49) 53 (38)

* Column percentage.

Statistical Analysis

The data were evaluated using the SPSS statistical package, version 11

(SPSS, Chicago, IL). The percentage and mean � standard deviation

values were calculated for descriptive statistics. A chi-square test was

used for intergroup comparisons, and logistic regression analysis (back-

ward method) was used for multivariate analysis. The risk was presented

as the odds ratio (OR) and 95% confidence interval (CI). The level of

statistical significance was set at P < 0.05.

Results

This cross-sectional descriptive study included 259 chil-

dren, of whom 147 (57%) were male, for a male:female ra-

tio of 1.3:1. The mean age overall was 33.08 � 18.97

months (range, 6-84 months). The mean age of the 140 chil-

dren with recurrent febrile seizures was 38.22 � 19.44

months. Of these 140 children, 80 (57%) were male, for

a male:female ratio of 1.2:1.

Sociodemographic features and the distribution of risk

factors for children with and without recurrent febrile sei-

zures are presented in Table 1.

Of the 259 children, 33 (12.7%) were diagnosed with

complex febrile seizures. The incidence of complex febrile

seizures was as follows: seizures lasting less than 15 min-

utes occurred in 34 cases; focal seizures occurred in 13

cases; and two or more seizures within the same day

occurred in 8 cases. Seizures recurred in 140 of the 259

cases (54%).

178 PEDIATRIC NEUROLOGY Vol. 43 No. 3

There was no statistically significant difference between

children with and without recurrent febrile seizures with

respect to sex, level of fever during the seizure, whether

the seizure was complex, and age at first seizure (Table

1). There was also no significant difference for parental

education, consanguinity, type of family, cause of fever,

any history of hospitalization in the neonatal intensive

care unit, and duration of seizure (data not shown).

In the present study, having a seizure with a low fever oc-

curred in 75 of 140 cases with recurrent febrile seizures

(54%) and in 69 of 119 cases without recurrent febrile

seizures (58%) (P = 0.747).

Among the cases with recurrent febrile seizures, 22% had

a seizure within the first hour of the febrile episode and

78% had a seizure after the first hour of the febrile episode.

The first seizure occurred at #18 months of age in 87 of

140 cases with recurrent febrile seizures (62%) and in 61 of

119 cases without recurrence (51%) (P = 0.078).

There were no statistically significant differences be-

tween the cases with and without recurrent febrile seizures

with respect to the seizures that had focal characteristics

(P = 0.558), lasted more than 15 minutes (P = 0.431), or

recurred during the same illness (P = 0.626). Among the

140 patients with recurrent febrile seizures, 17 (12%)

0

5

10

15

20

25

30

35

40

45

50

3 4 5 6 7 8

Number of risk factors

Number of cases

Figure 1. Distribution of multiple risk factors among 140 cases ofrecurrent febrile seizures. The maximum number of risk factors is nine(listed in Table 1).

Table 2. The nine risk factors for recurrence of febrile seizures

according to logistic regression analysis

Risk Factors P value Odds Ratio

95%

Confidence

Interval

Sex: Female* vs Male 0.627 1.144 0.665-1.968

Domicile: Urban* vs Nonurban 0.001 2.942 1.516-5.709

Income level: # Subsistence wage*

vs > Subsistence wage

0.013 2.766 1.234-6.197

Family history of febrile seizures:

Negative* vs Positive

0.018 1.933 1.121-3.333

Family history of epilepsy:

Negative* vs Positive

0.129 2.110 0.804-5.539

Level of fever: #39�C* vs >39�C 0.653 1.132 0.659-1.945

Duration of fever before seizure:

#1 hour* vs >1 hour

0.054 1.876 0.988-3.563

Complex febrile seizure: Positive*

vs Negative

0.553 1.281 0.565-2.906

Age at seizure onset: #18 months

vs >18 months*

0.105 1.565 0.910-2.691

* Reference category.

had complex febrile seizures. There was no significant

difference between patients with and without recurrent

febrile seizures with respect to complex febrile seizures

(P = 0.754).

Of the 140 patients with recurrent febrile seizures, 41

(55%) had 3 or more recurrences (range, 3-12). The sex

ratio for this subset was the same as for the full sample of

140 (i.e., a male:female ratio of 1.2:1).

Recurrent febrile seizures were significantly higher in

cases with nonurban domicile, compared with urban domicile

(P = 0.012). The recurrence rate in the children of families

with an income level greater than the subsistence wage level

(91%) was significantly higher than for those with a family

income level below the subsistence level (9%) (P = 0.005).

The recurrence rate of febrile seizures was significantly

higher in children with a positive family history of febrile

seizures (57%), compared with those without such a family

history (44%) (P = 0.031) (Table 1). For those with a his-

tory of febrile seizures among first degree relatives, the

rates were 36% for cases with recurrent febrile seizures

and 27.2% for cases without, respectively, whereas the

rates were 21% and 20% among second degree relatives,

respectively (P = 0.581). In addition, the recurrence rate

of febrile seizures was 58% in cases with a family history

of febrile seizures in one relative, and 65.9% in those with

a family history of febrile seizures in two or more rela-

tives (P = 0.378).

A positive family history of epilepsy was significantly

higher in children with recurrent febrile seizures, compared

with those without recurrent febrile seizures (P = 0.027).

Multiple risk factors for recurrent febrile seizures in chil-

dren occurred as follows (these data are also presented

graphically in Fig 1): three of the nine risk factors in 12

cases (8.6%), four risk factors in 29 cases (20.7%), five

risk factors in 43 cases (30.7%), six risk factors in 36 cases

(25.7%), seven risk factors in 16 cases (11.4%), and eight

risk factors in 4 cases (2.9%).

In the present study, according to the results of multi-

variate logistic regression analysis, nonurban domicile

(OR = 2.942; 95% CI = 1.516-5.709), having an

income over the subsistence wage (OR = 2.766; 95%

CI = 1.234-6.197), and a family history of febrile seizures

(OR = 1.933; 95% CI = 1.121-3.333) were significant

risk factors for recurrent febrile seizures. However, a fam-

ily history of epilepsy (OR = 2.110; 95% CI = 0.804-

5.539) and having the seizure after the first hour of the

febrile illness (OR = 1.876; 95% CI = 0.988-3.563)

were not a significant risk factor (Table 2).

Five risk factors (nonurban domicile, income greater than

the subsistence wage, a positive family history of febrile

seizures, a positive family history of epilepsy, and having

the seizure after the first hour of the febrile illness) contrib-

uted to a statistically significant difference in cases with re-

current febrile seizures, compared with those without

a recurrence (Table 1), but did not contribute to a significant

difference between cases with a single recurrence and those

with two or more recurrences (Table 3).

Discussion

The course of febrile seizures in childhood is usually be-

nign, and the long term prognosis is good; however, febrile

seizures recur in one third of cases, and three or more recur-

rences are observed in approximately 10% of cases. Many

risk factors have been studied and identified for recurrence

[1,3,7,8,16]. The most frequently reported risk factors are

a family history of febrile seizures, young age at seizure

onset, having seizures with a relatively low fever, and

shorter duration of fever before the seizures. A family

history of epilepsy and the peak temperature during the

febrile seizure are still controversial risk factors [1,7,10].

From a large number of international studies, it has been

reported that a family history of febrile seizures is a power-

ful prognostic risk factor for recurrent febrile seizures,

and the risk increases with the number of relatives

who have that history [4,6,7,9,10,17-20]. Approximately

Tosun et al: Risk Factors in Febrile Seizures 179

Table 3. Risk factors in recurrent febrile seizures patients by

number of recurrences

Risk Factors

Patients with

1 recurrence,

no. (%)*

Patients with $2

recurrences,

no. (%)* P-value

Sample size n = 66 n = 74

Sex

Male 38 (58) 42 (57) 0.922

Female 28 (42) 32 (43)

Domicile

Urban 49 (70) 49 (66) 0.660

Nonurban 25 (30) 25 (34)

Income level

# Subsistence wage* 5 (8) 8 (11) 0.510

> Subsistence wage 61 (92) 66 (90)

Family history of febrile seizures†

Positive (n = 132) 41 (62) 39 (53) 0.261

Negative (n = 127) 25 (38) 35 (47)

Family history of epilepsy

Positive 11 (17) 9 (12) 0.447

Negative 55 (83) 65 (88)

Level of fever

#39�C 35 (53) 40 (54) 0.631

>39�C 30 (45) 29 (39)

Duration of fever before seizure

# 1 hour 10 (16) 18 (24) 0.151

> 1 hour 54 (84) 52 (66)

Complex febrile seizure

Positive 9 (14) 8 (11) 0.609

Negative 57 (86) 66 (89)

Age at seizure onset

#18 months 37 (56) 50 (68) 0.161

>18 months 29 (44) 24 (32)

* Reference category.† Sample size given is the total number of family members in that

category, excluding the patient cohort.

25-40% of children with febrile seizures had a positive

family history of febrile seizures, and the risk of

developing febrile seizures among their siblings was

reported as 9-22% [4,7,19]. In accord with similar reports

[5,10,17,18,21,22], in the present study a positive family

history of febrile seizures was significantly higher in

children with recurrent febrile seizures, compared with

those without recurrent febrile seizures (P = 0.031).

Rantala and Uhari [23] reported that a family history of

febrile seizures was not a risk factor for recurrent febrile

seizures, whereas a history of febrile seizures among the

first degree relatives was significant. Van Esch et al. [19]

reported that a history of febrile seizures among the first de-

gree relatives increased the risk of recurrent febrile seizures;

however, the presence of febrile seizures among second de-

gree relatives was not a significant risk factor for recurrent

febrile seizures. In the present study, the rates of febrile sei-

zures among first degree and second degree relatives were

similar, at 62.5% and 58%, respectively; however, a positive

history of febrile seizures among first degree relatives was

not a significant risk factor (P = 0.581). The recurrence

rate of febrile seizures increased with the increase in the

180 PEDIATRIC NEUROLOGY Vol. 43 No. 3

number of family members with a history of febrile sei-

zures; however, the difference was not statistically signifi-

cant (P = 0.378). The present findings indicate that

a family history of febrile seizures is the most important

risk factor (OR = 1.933; 95% CI = 1.121-3.333).

Based on many studies, a positive family history of

epilepsy is still controversial as a risk factor for recurrent fe-

brile seizures. From a few studies, it was reported that a fam-

ily history of epilepsy moderately increases in the risk of

febrile seizure recurrence [5,14]. In contrast, other studies

revealed no difference in recurrence risk between children

with and without a family history of epilepsy [1,9-11,21].

In yet other reports, a family history of epilepsy is listed

either among probable or among certain risk factors for

recurrent febrile seizures [1,8,9,12,24]. In the present

study, a positive family history of epilepsy was found in

greater proportion among children with recurrent febrile

seizures than among those without recurrence (P =

0.027). Nonetheless, family history of epilepsy in cases

with recurrent febrile seizures was not a significant risk

factor according to multivariate logistic regression

analysis (P = 0.129; OR = 2.110; 95% CI = 0.804-5.539).

A relationship has been reported between age at onset of

febrile seizures and recurrence of febrile seizures

[2,3,9,12,17,25]. In the meta-analysis by Berg et al. [17],

it was demonstrated in 12 of 14 studies that febrile seizures

at early ages increase rates of recurrence. A first febrile sei-

zure at less than 18 months of age and a family history of

febrile seizures are reported to be the strongest and the

most consistent risk factors for recurrent febrile seizures

[1,5,9,12,17,21]. Berg et al. [12] reported the risk of recur-

rence within 1 year as 30% for cases with the first febrile

seizure at less than 18 months of age, and as 18% for those

with their first febrile seizure later than that.

Some authors consider young age to be associated with

a lower threshold for febrile seizures [25], whereas others

explain the association on the basis of the potential for

more febrile disease at this age [12,20,23,26]. Uran

et al. [27] reported that the onset of febrile seizures before

the age of 1 year was a significant risk factor for recur-

rence. However, in the present study, and similar to the

findings of Rantala and Uhari [23] and Tarkka et al.

[11], age at onset of febrile seizures was not a significant

risk factor for recurrent febrile seizures (P = 0.078).

Although the definition of febrile seizures includes the

presence of fever, there is no current evidence on the

level of fever required for a diagnosis of febrile seizures

[4]. Most febrile seizures occur either early or late in the

course of illness, and may be the primary cause for

hospital admission in approximately 25-50% of cases

[4,7,13,24]. Despite the common belief that the rate of

rise in temperature is more important for the development

of a febrile seizure than the level of fever as such, there is

no evidence to support this hypothesis [4,7,24,28].

From many studies, it has been reported that a relatively

low temperature increases the rate of recurrent febrile

seizures [1,9,10,12,18,29]. Methodologic problems remain,

however, including the degree of fever defined for febrile

seizures, the measurements of fever (axillary or rectal), the

time of temperature measurement (before the seizure or at

the time of seizure), measuring the temperature at home or

in the emergency department, interventions (e.g.,

antipyretics or warm baths) to lower the fever performed

prior to hospital admission, and recording the temperature

accurately (�F or �C units) [4,7,9]. It has been suggested

that a diagnosis of febrile seizures should be based on

medical history and physical examination findings alone,

because it is not practical to determine of the level of fever

required to diagnose a febrile seizure. This suggestion is in

accord with the recommendations of the National Institutes

of Health [15].

In the present study, low fever was defined as axillary

temperature of 39�C or less. Low fever at the initial febrile

seizure was observed in 75 of the 140 cases with recurrence

of febrile seizure (54%) and in 69 of the 119 cases without

recurrence (58%); the difference was not significant

(P = 0.747). Although much of the literature does indicate

some association between fever and recurrence of febrile

seizures, results from several studies support the present

negative findings [11,14,18,23].

The duration of fever before a febrile seizure is an impor-

tant risk factor for recurrence of febrile seizures. The shorter

the duration of fever prior to the seizure, the greater the risk

for recurrence [1,3,13]. Berg et al. [12] reported febrile sei-

zure recurrence rates as follows: 44% in cases with a fever

duration of less than 1 hour before a febrile seizure, 23% in

cases with a fever duration of 1-24 hours, and 13% in sub-

jects with a fever duration greater than 24 hours. Pavlidou

et al. [10] found that recurrence rates of febrile seizures

were significantly higher for cases with a febrile seizure

within the first 12 hours of the febrile episode, compared

with a seizure between hours 12 and 24 hours; this signifi-

cance disappeared as the number of recurrences increased.

In the present study, the recurrence rate was significantly

higher in cases with a fever duration of less than 1 hour prior

to the febrile seizure (P = 0.017). No significant difference

could be established in terms of a single recurrence and

multiple recurrences of febrile seizures. Similarly, Chung

et al. [18] did not find a significant relationship between

the duration of fever prior to the febrile seizure and

recurrence of febrile seizures.

In the present study, nonurban domicile was one of the

risk factors for recurrence of febrile seizures (P = 0.012),

probably due to due to difficulties in reaching a health cen-

ter during the febrile episode. In addition, the level of ma-

ternal education was primary school or lower in 36% of

the cases with recurrence of febrile seizures (and in 20%

of the cases, for paternal education), but this was not statis-

tically significant. Similarly, for nonurban domicile the ma-

ternal of education was primary school or lower in 54% of

the cases (and 36%, for paternal education). This finding

may reflect the inadequate knowledge of parents about mea-

suring, evaluating, and lowering the child’s temperature

during the course of a febrile episode.

In the present study, the recurrence rate was significantly

higher in the children of families with an income level

above the subsistence wage, compared with those with an

income level below the subsistence wage (91% and 9%, re-

spectively) (P = 0.005). These findings may be explained by

fewer hospital admissions for patients with income level be-

low subsistence, and by the absence of social security, and

also by more hospital admissions for patients with income

above subsistence wage (influenced by, for example, avail-

ability of private cars, as well as a high economic status and

consciousness about the disease).

Aydin et al. [30] found that socioeconomic status and the

level of paternal education were significantly lower in

patients with febrile seizures, Forsgren et al. [31] reported

the level of maternal education as a risk factor. In the present

study, the level of maternal education was primary school or

lower in 43% of the cases with multiple recurrence of febrile

seizures, but this was not statistically significant.

Sex, ethnic origin, complex febrile seizures, and patho-

logic findings on neurologic examination were not among

the risk factors for recurrence of febrile seizures identified

by Shinnar and Glauser [1]. In the present study, both fe-

brile seizure and recurrence were more frequent in male

than in female cases (male:female ratios of 1.3:1 and

1.2:1, respectively). This finding is in accord with many

other studies [10,11,18,22]. The sex ratio for cases with

recurrence did not vary between isolated recurrence and

three or more recurrences, but remained constant at 1.2:1.

Recurrence of febrile seizures is more frequently encoun-

tered in children who had complex febrile seizures [32].

Nonetheless, and in accord with the present findings, there

are also studies demonstrating no relationship between

complex febrile seizures and the risk for recurrence of fe-

brile seizures [12,23].

Thus, although febrile seizures are the most frequently

observed seizures of childhood and have a good prognosis,

it is important for clinicians to know the potential risk factors

for recurrence. The present cross-sectional study determined

the risk ratios for recurrence of febrile seizures in a Turkish

population. Additional studies should be designed using the

defined risk ratios in a scoring model for children with

febrile seizures in a longitudinal prospective study.

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