Seizure: European Journal of Epilepsy 80 (2020) 24–30

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Seizure: European Journal of Epilepsy

journal homepage: www.elsevier.com/locate/seizure

Importance of prompt diagnosis in pediatric epilepsy outcomes T

a a b,c,
Asma Khan , Hyun Lim , Salah Almubarak *
a
Department of Community Health and Epidemiology, University of Saskatchewan, Box 7, Health Science Building, 107 Wiggins Road, Saskatoon, SK S7N 5E5, Canada
b
Department of Pediatrics, Neurology Division, Royal University Hospital, Royal University Hospital, 103 Hospital Dr, Saskatoon, SK S7N 0W8, Canada
c
Department of Pediatrics, Neurology Division, Qatif Central Hospital, Qatif, Saudi Arabia, Dhahran Jubail Rd, Qatif, Eastern Province, 32654, Saudi Arabia

ARTICLE INFO ABSTRACT

Keywords: Purpose: Recognition of childhood epilepsy has improved worldwide. Children with epilepsy require immediate
Epilepsy outcome healthcare evaluation and monitoring. The interval between the onset of the first seizures and pediatric neu-
Developmental outcome rology assessment may influence the epilepsy outcome at follow-up assessments. This study aimed to assess the
Waiting time of evaluation quality of medical care for children with first seizure onset and determine the impact of pediatric neurology
clinic waiting times on epilepsy outcomes.
Methods: This was a retrospective cohort study based on chart reviews and included patients who underwent
their first seizure evaluation at the Royal University Hospital in Saskatoon, Canada between January 1, 2012 and
December 31, 2015. Waiting time (the time interval between seizure onset and the first clinical assessment) and
baseline factors were examined in relation to epilepsy outcome on follow-up.
Results: Of a total 1157 patients evaluated for epilepsy for the period 2012–2015, 197 patients had unprovoked
seizures and were eligible for this study. The mean age of the patients at seizure onset was 5.6 ( ± 5.1) years. The
mean waiting time was 4.33 months and the mean follow-up time was 20.9 months. Shorter waiting times in the
clinic led to a more favourable seizure outcome. Of the 197 assessed at the last seizure assessment, 132 (67 %)
patients had a favourable epilepsy outcome with no seizures at follow-up appointments and 65 (33 %) showed
an unfavourable epilepsy outcome with persistent seizures at follow-up appointments.
Conclusion: Early assessment of first seizure onset is crucial for the management of children with epilepsy.
Waiting time and other factors may influence epilepsy outcome, and represent opportunities to improve standard
medical care.

1. Introduction
Epilepsy is one of the most common neurological disorders affecting
individuals worldwide [1]. Every year in Canada, 15,500 individuals
are diagnosed with epilepsy [2]. The incidence of pediatric epilepsy in
Canada is 41 per 100,000 children per year [3]. The diagnosis of
childhood epilepsy can involve a lengthy waiting period between the
first seizure and the first appointment with a medical professional. In
emergency situations, patients can receive medical assessment by a
physician who is not specialized. However, longer-term treatment and
management are typically performed by a pediatric neurologist. This
process requires time, which has an added impact on epileptic patient
management. The impact of waiting times in childhood epilepsy on
child development is crucial to understand since this is a critical period
of brain development and maturation. Our study observed the waiting
times of pediatric epilepsy patients and their resulting epilepsy out-
comes.
The first clinic visit after seizure onset is crucial as the appointment
confirms seizure diagnosis, initiates appropriate management of the
illness, and counsels parents about their concerns regarding the newly
diagnosed child [4]. The burden of an epilepsy diagnosis is usually
borne by the parents, causing additional stress and a significantly af-
fecting parental quality of life [5–8]. In Saskatchewan, the vulnerable
populations that have limited access to medical resources make self-
management difficult. This necessitates an increased usage of other
specialized health care resources, including emergency departments, or
surgery [9]. This leads to a less optimal quality of life for all concerned
including the patient, caregiver, and clinicians. Specifically, in a study
assessing the effects of lengthened waiting times in pediatric epilepsy
on the development of children, patient developmental outcomes were
found to be poor in those whose appointments were delayed by over a
month [10]. Our study looked at similar outcomes and documented
similar results.
Clement and Wallace [11] associated motor, language, and

⁎
Corresponding author.
E-mail addresses: aak770@mail.usask.ca (A. Khan), hyun.lim@usask.ca (H. Lim), s.almubarak@usask.ca (S. Almubarak).

https://doi.org/10.1016/j.seizure.2020.03.011
Received 15 July 2019; Received in revised form 2 March 2020; Accepted 23 March 2020
1059-1311/ © 2020 Published by Elsevier Ltd on behalf of British Epilepsy Association.
A. Khan, et al.
Fig. 1. Study Flow depicting the selection of children with epilepsy seen between January 1, 2012 and December 31, 2015.
behavioral outcomes with the impact of waiting time for medical at-
tention in children with epilepsy, but their study only included 34
adolescents, a very small sample. Another similar study detected a re-
lationship between developmental disabilities and the prevalence of
epilepsy but being a cross-sectional study, it was difficult to draw causal
associations [12]. Other studies also showed that persistent seizures
caused developmental delays in children [13–15,11,16–19]). There are
very few studies in Canada that have assessed waiting times at seizure
clinics for adults [20]. However, even fewer studies have evaluated the
effects of waiting times and other factors on epilepsy outcomes in pe-
diatric neurological practice.
Thus, it is important to have a comprehensive understanding of the
factors associated with waiting time in a pediatric epilepsy clinic. This
study aimed to investigate the associations underlying epilepsy out-
comes in a hospital-based sample of children with epilepsy. The ob-
served variables included child age, age at seizure onset, sex, residence,
waiting time, type of epilepsy, seizure frequency, and treatment. Our
study examines the impact that the waiting time has on epilepsy out-
come. In our study, waiting time is defined as the time lapse between
seizure onset and the first clinic appointment for diagnosis by a pe-
diatric neurologist. Our study hypothesis is that shorter waiting time
periods lead to an improved epilepsy outcome.
2. Methods
This retrospective cohort study was completed at the Royal
University Hospital in Saskatoon, Saskatchewan, Canada. Approval to
participate in the study was obtained from the University of
Saskatchewan and permission to complete the data collection of in this
study was obtained from the Saskatoon Health Region research ethics
review board in 2015. The privacy of the participant was protected by
removing all personal health information that was not required for the
purposes of the research and there was no waiver of informed consent
as per the Institute’s Ethics Board. The Royal University Hospital is the
only tertiary hospital in the province of Saskatchewan that has all of the
subspecialty clinics including pediatric epilepsy care for individuals
25
Seizure: European Journal of Epilepsy 80 (2020) 24–30
aged leas than 17 years old. The hospital is based in Saskatoon as it is
the most populous urban center in Saskatchewan, centrally located
within the province. In 2012, the epilepsy clinic had limited resources
and was staffed with only one pediatric neurologist. The number of
practicing pediatric neurologists increased from one to two specialists
in 2013. This increased further from two to three pediatric neurologists
in 2014, and in 2015, the team stabilized with four pediatric neurolo-
gists.
All pediatric patients that were included in this study attended at
least one appointment with a pediatric neurologist at the epilepsy clinic
between January 1, 2012 and December 31, 2015 at the Royal
University Hospital and the outreach clinic in Regina. When inclusion/
exclusion criteria were considered, and following the International
League Against Epilepsy (ILAE) definitions and classification for epi-
lepsy, 197 pediatric patients were eligible and included in all analyses.
The selection of patients that were considered in this study can be
viewed in Fig. 1.
Data were collected through electronic medical chart review at the
Saskatoon Health Region and data included information regarding de-
mographics characteristics, and clinical seizures presentation. Further,
both language and gait development outcome was assessed at first
clinic and follow-up appointments according to the pediatric neurolo-
gist as being age-appropriate or delayed. Finally, epilepsy outcome was
assessed at specific monthly periods in magnitudes of 6-month, 12-
month, and 18-month follow-up investigations. The province of
Saskatchewan differs significantly from other provinces by population
density. In this study, rural was defined as distance over 240 km away
from the pediatric neurology clinic, and any town within 240 km of the
clinic was considered urban.
Median and mean waiting times for an official diagnosis were de-
termined. Further, the outcomes at the final follow-up appointment by
the pediatric neurologist were compared to those at the initial diagnosis
by a pediatric neurologist. An unfavourable outcome was ascertained in
patients who continued to have seizures at follow-up and a favourable
outcome was ascertained in patients who experienced no seizures at
follow-up appointments. All analyses were performed using SPSS
 Table 1
Demographic data distribution (N = 197).
A. Khan, et al.

n % ± SD Range n % ± SD Range n % ± SD Range n % ± SD

Sex
Male (N = 107) 20 18.7 % 23 21.5 % 17 15.9 % 14 13.1 %
Female (N = 90) 20 22.2 % 16 17.8 % 14 15.5 % 8 8.9 %
Residence
Urban (N = 77) 12 15.6 % 14 18.2 % 10 13.0 % 13 16.9 %
Rural (N = 120) 27 22.5% 16 13.3% 22 18.3% 18 15.0%
Mean Age at Diagnosis (years) 2.6 ± 2.2 0–3 2.3 ± 1.9 0-–3 8.8 ± 8.6 3–15 8.1 ± 7.6
Seizure Type
Focal (N = 136) 21 15.4 % 26 19.1 % 20 14.7 % 23 16.9 %
Generalized (N = 61) 10 16.4 % 12 19.7 % 8 13.1 % 12 19.7 %
Gait Delay (N = 24) 4 16.8 % 2 8.3 % 0 0.0 % 5 20.8 %
Language Delay (N = 38) 5 13.2% 7 18.4% 1 2.6 % 6 15.8%
Etiology
Unidentified (N = 89) 15 16.9 % 17 19.1 % 11 12.4 % 11 12.4 %
Genetic (N = 70) 14 20.0 % 12 17.1 % 8 11.4 % 15 21.4 %
Structural (N = 38) 8 21.1 % 6 15.8 % 9 23.6 % 4 10.5 %
Median Number of Anti-Seizure Medications
Total 3 ± 2.6 0–4 1 ± 0.7 1–2 1 ± 0.6 0–2 1 ± 0.5
Before First Visit 0 1 ± 0.8 0-1 1 ± 0.7 0-1 0
Epilepsy Surgery (N = 7) 1 14.3 % 0 0.0 % 3 42.9 % 2 28.6 %
Ketogenic Diet (N = 21) 0 0.0 % 5 23.8 % 5 23.8 % 3 14.3 %
Median Number of Visits 5 ± 3.4 2–11 7 ± 4.6 3–16 2 ± 1.2 1–7 3 ± 1.3
Median Waiting Time (months) 2 ± 1.6 0–4 1 ± 0.8 0–3 5 ± 4.8 1–10 3 ± 2.7
Median Follow-up Duration (months) 24 ± 15.4 6–22 21 ± 11.7 7–35 20 ± 9.8 2–27 18 ± 10.8

26
Range n % ± SD Range n % ± SD Range n % ± SD Range n % ± SD Range

Sex
Male (N = 107) 10 9.3 % 8 7.5 % 6 5.6 % 9 8.4 %
Female (N = 90) 13 14.4 % 5 5.6 % 5 5.6 % 9 10.0 %
Residence
Urban (N = 77) 4 5.2 % 7 9.1 % 9 11.7 % 8 10.3 %
Rural (N = 120) 15 12.5% 11 9.2 % 6 5.0 % 5 4.2 %
Mean Age at Diagnosis (years) 3–13 1.7 ± 1.1 0–3 2.2 ± 1.4 0–3 8.5 ± 7.2 3–12 8.3 ± 7.0 3–14
Seizure Type
Focal (N = 136) 12 8.8 % 13 9.7 % 9 6.6 % 12 8.8 %
Generalized (N = 61) 4 6.6 % 6 9.8 % 3 4.9 % 6 9.8 %
Gait Delay (N = 24) 3 12.5 % 5 20.8 % 3 12.5 % 2 8.3 %
Language Delay (N = 38) 4 10.5% 6 15.8% 4 10.5% 5 13.2%
Etiology
Unidentified (N = 89) 6 6.7 % 7 7.9 % 9 10.1 % 13 14.5 %
Genetic (N = 70) 5 7.1 % 8 11.4 % 2 3.0 % 6 8.6 %
Structural (N = 38) 3 7.9 % 2 5.3 % 4 10.5 % 2 5.3 %
Median Number of Anti-Seizure Medications
Total 1–3 1 ± 0.4 1–3 2 ± 1.5 1–6 2 ± 1.6 1–5 2 ± 1.3 1–9
Before First Visit 1 ± 0.8 0-2 0 1 ± 0.7 0-1 0
Epilepsy Surgery (N = 7) 0 0.0 % 1 14.3 % 0 0.0 % 0; 0.0 % 0 0.0 %
Ketogenic Diet (N = 21) 1 4.8 % 0 0.0 % 4 19.0 % 4; 19.0 % 3 14.3 %
Median Number of Visits 2–12 5 ± 2.5 3–14 4 ± 2.2 3–24 3 ± 1.8 2–19 3 ± 1.4 2–21
Median Waiting Time (months) 0–6 4 ± 3.2 0–5 3 ± 2.1 0–9 6 ± 4.8 0–24 6 ± 5.0 0–11
Median Follow-up Duration (months) 3–28 21 ± 14.2 5–40 23 ± 16.4 6–54 19 ± 12.9 5–39 18 ± 11.8 8–42

N = sample within demographic data subgroup; n = sample within epilepsy outcome by demographic data; % = n/N; SD = Standard deviation (provided where appropriate).
Seizure: European Journal of Epilepsy 80 (2020) 24–30
A. Khan, et al. Seizure: European Journal of Epilepsy 80 (2020) 24–30

Table 2 at the seizure clinic between 2012 and 2015 in this study is showed in
Epilepsy characteristics of the study sample (N = 197). Fig. 2. The table displays the number of patients, the number of pe-
diatric neurologists, and minimum, mean, and maximum waiting times
Variable Mean N (%); ( ± SD); (Range)
in months by year. There are patients that were referred from different
Seizure type subspecialties such as Family Physicians, Pediatricians, Emergency
Focal 136 (69 %) Rooms, etc. Some patients included in this study have been seen im-
Generalized 61 (31 %) mediately and some patients have been referred from pediatric emer-
Etiology
gency without being seen immediately. However, both types of patients
Unidentified / Others 89 (45 %)
Genetic 70 (36 %) have been included in our study. Thus, there are minimum waiting
Structural 38 (19 %) times in 2012, 2013, and 2015 of patients with minimal waiting times.
Seizure frequency Average waiting time was the longest in 2014 as the maximum waiting
< 10 52 (26 %)
time was longest in that cohort year at 24 months, but the number of
> 10 145 (74 %)
Treatment
patients in 2014 was also double of that in 2012. In 2015, the number
Anti-seizure medication 196 (99 %) (0–9) of patients was higher than in years 2012 or 2013 but the waiting time
Ketogenic diet 21 (11 %) was at its lowest across the study period. Further, the number of pe-
Surgery 7 (4 %) diatric neurologists gradually increased from 1 to 4 within the study
Waiting time (months) 4.33 ( ± 3.6)(0–24)
period from one in 2012 to four neurologist in 2014. In 2015, waiting
Follow-up period (months) 20.9 ( ± 11.0)(2.4–54.0)
times were the shortest and the clinic was also staffed with the max-
imum number of pediatric neurologists during the study period. On
version 23.0. average during the course of this study, urban residents waited 3.6
months and rural residents waited 5.5 months for first clinic appoint-
3. Results ment.

3.1. Demographics and clinical characteristics

3.2. Developmental outcome
In our study of 197 patients, we looked at a descriptive analysis of
Table 3 presents developmental information for the 197 pediatric
factors under observation in our study by age, epilepsy outcome, and
epilepsy patients who were diagnosed with seizures in this study. Their
seizure frequency. This is depicted in Table 1. Further, in Table 1 the
development is described in terms of gait as “age-appropriate” and
data is described as having lengthier waiting times in months for those
“delayed” and the patients’ language skills as “age-appropriate” and
with fewer seizures.
“delayed”. Additionally, data on patient development at the final
Of 197 patients, 90 (46 %) were female and 120 (61 %) resided
follow-up appointments are also presented in this table. There were 2
outside of the Saskatoon Health Region. Epilepsy was diagnosed in the
fewer patients with gait development difficulties and 4 fewer patients
first year of life in 37/197 (19 %) children. The mean age at diagnosis
with language development difficulties at the final follow-up appoint-
of our study participants was 6.2 years, ranging from 2 to 16 years old.
ment. Further, 3 fewer patients ended up having both a gait and lan-
The mean age at seizure onset was 5.6 which ranged between 0–16
guage difficulty and 9 more patients were at their age-appropriate
years old.
milestones for gait and language development in the last year of follow-
Anti-seizure medication was used for treatment in 196 (99 %) pa-
up.
tients, the number of drugs consumed by the patients over their clinical
course ranged from 0 to 9 anti-seizure medications. clinical presenta-
tion, treatment, and waiting time factors of the study sample are listed 3.3. Epilepsy outcome
in Table 2.
The waiting time for pediatric epilepsy patients who were diagnosed Epilepsy outcome was determined at the specific points in time of 6,

Fig. 2. Waiting time at pediatric seizure clinic from 2012 to 2015 (N = 197).

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A. Khan, et al. Seizure: European Journal of Epilepsy 80 (2020) 24–30

Table 3 Table 4
Developmental characteristics at initial and final follow-up (N = 197). Univariate logistic regression results for unfavourable epilepsy outcome at 6
months, 12 months, and 18 months follow-up (N = 197).
Variable Mean N (%)
6 months
Development at diagnosis
Delayed gait only 9 (5 %) Variable OR 95 % CI p-value
Delayed language only 23 (12 %)
Delayed gait and language 15 (8 %) Sex
Age-appropriate 150 (76 %) Male 1
Development at last follow-up Female 1.14 0.65–2.00 0.65
Delayed gait only 7 (3 %) Age at seizure onset 1.01 0.95–1.07 0.79
Delayed language only 19 (9 %) Age at diagnosis 1.03 0.51–1.09 0.34
Delayed gait and language 12 (6 %) Residence
Age-appropriate 159 (81 %) Urban 1
Rural 1.39 0.78–2.47 0.26
Gait
12, and 18-month follow-up appointments with all odds ratios calcu- Age-appropriate 1
lated at the 6-month follow-up appointment, the 12-month follow-up, Delayed 2.96 1.17–7.50 0.02*
Language skills
and the 18-month follow-up as labelled in Table 4. Patients were coded
Age-appropriate 1
as either having persistent seizures or no further seizures at these three Delayed 2.13 1.02–4.41 0.04*
points in time. Univariate logistic regression analysis results of a poor Type of epilepsy
epilepsy outcome is displayed in Table 4 gait, language, and waiting Focal 1
time were consistently significant in each univariate model. The total Generalized 0.7 0.38–1.27 0.24
Etiology
number of anti-seizure medications was a significant predictor of poor
Unidentified 1
epilepsy outcome in the 18-month model (p = 0.05). Genetic 0.8 0.36–1.75 0.57
Table 5 presents the results of multivariate logistic regression with Structural 1.02 0.48–2.19 0.95
odds ratios provided based on the specific time points of the 6-month Number of anti-seizure medications before first 0.92 0.65–1.32 0.66
clinic
follow-up appointment, the 12-month follow-up appointment, and the
Total number of anti-seizure medications 1.09 0.87–1.37 0.45
18-month follow-up appointment. Gait and waiting time were both EEG 0.65 0.36–1.19 0.16
consistently significant factors in this analysis. The total number of anti- Ketogenic diet 1.5 0.60–3.73 0.39
seizure medications was only significant in the 18-month model after Surgery 1.45 0.32–6.66 0.63
controlling for gait and waiting time (OR = 1.36; 95 % C.I: 1.10–1.75; Number of visits 0.95 0.84–1.07 0.37
Duration of follow-up visits (months) 1.02 0.99–1.04 0.22
p-value = 0.02). Moreover, gait that was delayed at 6 months, 12,
Waiting time (months) 1.12 1.04–1.22 0.01*
months, and 18 months was associated with a higher risk of persistent
seizures at follow-up. At the 18 month follow-up investigation, a de-
12 months
layed gait was associated with a 3.1-fold higher risk of persistent sei-
zures when compared to a gait that was age-appropriate after control- Variable OR 95 % CI p-value
ling for the total number of anti-seizure medications and waiting time
(OR = 3.1; 95 % C.I: 1.25–7.70; p-value = 0.02). Our data did not show Sex
Male 1
both residency and waiting time covariates in the multivariate model, Female 1.16 0.65–2.07 0.61
thus we did not consider collinearity to be an issue in our findings. Age at seizure onset 0.98 0.93–1.04 0.58
Age at diagnosis 0.99 0.94–1.06 0.96
Residence
Urban 1
4. Discussion
Rural 1.52 0.85–2.74 0.16
Gait
Our results demonstrate that persistent seizures in pediatric patients Age-appropriate 1
with epilepsy are associated with both inherent characteristics of a Delayed 2.57 1.08–6.13 0.03*
child who experiences gait abnormalities and extrinsic characteristics of Language skills
Age-appropriate 1
care delivery such as the waiting time experienced before the child is
Delayed 2.1 1.03–4.30 0.04*
evaluated in an epilepsy clinic. Our data suggest that even for high risk Type of epilepsy
children with evidently abnormal neurological examinations, the epi- Focal 1
lepsy trajectory might be modified by enhancing access to appropriate Generalized 0.79 0.43–1.47 0.46
Etiology
care. This study showed that delayed gait and long waiting time were
Unidentified 1
associated with an unfavourable epilepsy outcome at 6 months, 12 Genetic 0.67 .30–1.52 0.34
months, and 18 months when observed independently. Gait delay and Structural 0.93 0.43–2.02 0.86
long waiting time were risk factors of an unfavourable epilepsy out- Number of anti-seizure medications before first 0.98 0.68–1.41 0.92
come when observed collectively. At the last follow-up, all groups that clinic
Total number of anti-seizure medications 1.17 0.93–1.47 0.17
previously experienced developmental difficulties improved to a level
EEG 1.22 0.65–2.27 0.53
that matched their peers. Most notably, 9 pediatric patients that pre- Ketogenic diet 1.55 0.63–3.86 0.34
viously had developmental delay in gait or language had age-appro- Surgery 2.24 0.49–10.27 0.3
priate developmental milestones on their last follow-up appointment Number of visits 1.01 0.90–1.13 0.92
Duration of follow-up visits (months) 1.01 0.99–1.04 0.4
and 7 of these patients had a favourable epilepsy outcome. Further, 2 of
Waiting time (months) 1.08 1.00–1.17 0.05*
these 9 patients were diagnosed in 2013, 4 were diagnosed in 2014, and
3 were diagnosed in 2015 with an average waiting time of 4 weeks. Our
18 months
findings support the results described in previous literature [21–23].
One unexpected finding of interest was the significance of the total Variable OR 95 % CI p-value
number of anti-seizure medications in the 18month follow-up for the
univariate and multivariate models. This is consistent with other studies (continued on next page)

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A. Khan, et al. Seizure: European Journal of Epilepsy 80 (2020) 24–30

Table 4 (continued) study showed that the residence was not significantly associated with
epilepsy outcome in logistic regression. Although the demographics of
18 months
our study population showed that a larger number of rural residents
Variable OR 95 % CI p-value had an unfavourable epilepsy outcome (37/65 patients, 57 %) in
comparison with patients who resided in urban areas (28/65 patients,
Sex 43 %), and rural residents waited 2 months more for a first clinic ap-
Male 1
pointment on average. In a previous study, no statistically significant
Female 1.04 0.63–2.05 0.68
Age at seizure onset 0.99 0.94–1.05 0.81 difference was observed between the urban and rural populations of the
Age at diagnosis 1.01 0.95–1.07 0.81 Manitoba province [26]. However, a higher prevalence was found in
Residence children of all ages living in lower socioeconomic neighborhoods in
Urban 1 urban areas [26]. Our study did not include information on parental
Rural 1.43 0.79–2.61 0.24
Gait
income but did show a higher prevalence of epilepsy amongst rural
Age-appropriate 1 children.
Delayed 2.6 1.10–6.19 0.03* We have anticipated several limitations during this study. It is a
Language skills retrospective study and there is restriction to the collected information.
Age-appropriate 1
Different physicians have been involved in this study and their ap-
Delayed 2.02 0.98–4.15 0.05*
Type of epilepsy proach has resulted in collection variable measures of information
Focal 1 during follow-up. A prospective design would have minimized this bias
Generalized 1.3 0.70–2.43 0.41 with more accuracy. Another limitation is that patients may not have
Etiology been referred to the Saskatoon Health Region pediatric neurology clinic
Unidentified 1
Genetic 0.99 0.42–2.32 0.99
or may have been misdiagnosed before seeking help at the clinic,
Structural 1.28 0.57–2.86 0.55 causing a bias in the sample size and lead to long waiting time. Some
Number of anti-seizure medications before first 0.94 0.64–1.37 0.73 patients were examined outside the province due to the lengthened
clinic waiting times during 2012 due to limited resources available in
Total number of anti-seizure medications 1.27 1.00–1.60 0.05*
Saskatchewan.
EEG 1.61 0.84–3.11 0.16
Ketogenic diet 1.53 0.61–3.83 0.37 This study also offered a number of strengths. It allowed for the
Surgery 1.48 0.32–6.80 0.62 observation of waiting time and location of residency in relation to
Number of visits 1 0.89–1.13 0.99 developmental and epilepsy outcomes in one single study. It also in-
Duration of Follow-up visits (months) 1.02 0.99–1.05 0.18 volved four cohort years of patients from 2012 to 2015. The presence of
Waiting time (months) 1.09 1.01–1.18 0.04*
only one centre that has the pediatric neurology clinics in
OR = odds ratio; CI = confidence interval; * = < .05 significance (p-value). Saskatchewan that evaluates clinical seizures in children and its central
location in Saskatoon allowed for appropriate representation of the
province and the inclusion of a large population sample, since all re-
that also assessed epilepsy outcomes in pediatric epilepsy patients ferrals are required to go through the single clinic. This made it easier
[24,25]. One study finding showed that consumption of as few as 3 or to generalize the findings for Saskatchewan and ensure that all patients
more drugs throughout the treatment led to a higher risk of drug re- went through the same clinical navigation system. Berg et al. [10]
sistance [24]. observed the impact of diagnostic delays on the development of pe-
Residence was not a significant predictor of epilepsy outcome. Our diatric epileptic patients in the state of Connecticut. It had two large
medical centers and 17 practicing pediatric neurologists with a popu-
Table 5 lation of 500,000 children at the time of the study, a much larger scale
Multivariate logistic regression results for unfavourable epilepsy outcome at 6 than was available in our study. Although different study designs were
months, 12 months, and 18 months follow-up (N = 197). utilized, our retrospective study is consistent with the results of Dr.
Berg’s prospective study. The association of epilepsy outcome in rela-
6 months
tion to waiting time and delayed language for children with epilepsy is
Variable OR 95 % CI p-value
present in both studies. Finally, it was also advantageous that the
Gait number of pediatric neurologists in the hospital grew from one spe-
Age-appropriate 1 cialist to four over the course of this study.
Delayed 3.15 1.22–8.13 0.02
This study illustrates the necessity for early recognition of epilepsy,
Waiting time (months) 1.13 1.04–1.23 < 0.001
measures the required resources for medical care, and treatment access
to pediatric medical care. The approaches for recognition and man-
12 months
agement of epilepsy that exist during 2012 required attention and more
Variable OR 95 % CI p-value
provided resources during 2013–2015 showed significant improve-
Gait ment; the results of this study can be used as a guide to the improve-
Age-appropriate 1 ment of epilepsy outcomes. Further research on understanding the
Delayed 2.66 1.11–6.42 0.03
disparities that exist among various populations with respect to waiting
Waiting time (months) 1.09 1.00–1.18 0.04
times is also recommended. Failure to ensure appropriate management
of children with epilepsy could be one reason for the continuity or re-
18 months
Variable OR 95 % CI p-value occurrence in adulthood and could explain the greater cost burden on
the health care system [4], this could be avoided by providing more
Gait resources for children with epilepsy [27]. More research is necessary in
Age-appropriate 1
order to support the findings of this study and to clearly define the ways
Delayed 3.1 1.25–7.70 0.02
Total number of anti-seizure medications 1.36 1.10–1.75 0.02 by which waiting times are affected. Additional prospective data and
Waiting time (months) 1.11 1.02–1.20 0.02 larger cohorts would be beneficial in exploring more effects of waiting
time in pediatric seizure clinics where patients are more comprehen-
OR = odds ratio; CI = confidence interval. sively evaluated for clinical variables and history of past seizures at the
point of diagnosis. These results could provide the foundation to

29
A. Khan, et al.
explore other health care inequalities among diverse marginalized po-
pulations.
5. Conclusion
Waiting time for seizure evaluation is correlated with epilepsy
outcome. Furthermore, it is a key factor in preventing developmental
delay. Prolonged waiting times for a pediatric neurology evaluation of
children with new onset epilepsy may augment the risk for a poor
epilepsy outcome. Early recognition of epilepsy, prompt referral to a
pediatric neurologist, and optimized access to specialty care may all
provide opportunities to improve the prognosis of children with epi-
lepsy. This study highlights the demands for clinical pediatric epilepsy
resources, emphasizes the importance of early evaluation and treat-
ment, and underscores the necessity of health services research for
children with epilepsy.
Declaration of Competing Interest
None.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.seizure.2020.03.011.
References
[1] World Health Organization. Epilepsy. 2018 Available from: http://www.who.int/
news-room/factsheets/detail/epilepsy. [Accessed February 8, 2019].
[2] Epilepsy Canada. Epilepsy facts. 2016 (Online). Markham, ON. Available from:
http://www.epilepsy.ca/epilepsyfacts.html [Accessed March 12, 2016].
[3] Camfield CS, Camfield PR, Gordon K, Wirrell E, Dooley JM. Incidence of epilepsy in
childhood and adolescence: a population-based study in Nova Scotia from 1977 to
1985. Epilepsia 1996;37(1):19–23.
[4] England MJ, Liverman CT, Schultz AM, Strawbridge LM. Epilepsy across the
Spectrum: promoting health and understanding. Washington, DC: National
Academies Press; 2012. p. 327–72.
[5] Benson A, Lambert V, Gallagher P, Shahwan A, Austin JK. Parent perspectives of the
challenging aspects of disclosing a child’s epilepsy diagnosis to others: why don’t
they tell? Chronic Illn 2017;13(1):28–48.
[6] Jones C, Reilly C. Parental anxiety in childhood epilepsy: a systematic review.
Epilepsia 2016;57(4):529–37.
[7] Ryan BL, Speechley KN, Levin SD, Stewart M. Parents’ and physicians’ perceptions
of childhood epilepsy. Seizure 2003;12(6):359–68.
[8] Saburi G. Stressors of caregivers of school-age children with epilepsy and use of
30
Seizure: European Journal of Epilepsy 80 (2020) 24–30
community resources. J Neurosci Nurs 2011;43:E1–12.
[9] Kenney MK, Mann MVA. Assessing systems of care for US children with epilepsy/
seizure disorder. Epilepsy Res Treat 2013:1–11.
[10] Berg AT, Loddenkemper T, Baca CB. Diagnostic delays in children with early-onset
epilepsy: impact, reasons, and opportunities to improve care. Epilepsia
2014;55(1):123–32.
[11] Clement MJ, Wallace SJ. A survey of adolescents with epilepsy. Dev Med Child
Neurol 1990;32(10):849–57.
[12] Prasad AN, Burneo JG, Corbett B. Epilepsy, comorbid conditions in Canadian
children: analysis of cross-sectional data from cycle 3 of the national longitudinal
study of children and youth. Seizure 2014;23(10):869–73. (2014).
[13] Allen NM, Conroy J, Deonna T, McCreary D, McGettigan P, Madigan C, Carter I,
Ennis S, Lynch SA, Shahwan A, King MD. Atypical benign partial epilepsy of
childhood with acquired neurocognitive, lexical semantic, and autistic spectrum
disorder. Epilepsy Behav Case Rep 2016;6:42–8.
[14] Beckung E, Uvebrant P. Motor and sensory impairments in children with intractable
epilepsy. Epilepsia 1993;34:924–9.
[15] Byars AW, Degrauw TJ, Johnson CS, Perkins SM, Fastenau PS, Dunn DW, et al.
Language and social functioning in children and adolescents with epilepsy. Epilepsy
Behav 2014;31:167–71.
[16] Kowulski K, Di Fabio RP. Gross motor and balance impairments in children and
adolescents with epilepsy. Dev Med Child Neurol 1995;37:604–19.
[17] Selassie GR, Viggedal G, Olsson I, Jennische M. Speech, language, and cognition in
preschool children with epilepsy. Dev Med Child Neurol 2008;50:432–8.
[18] Vanasse CM, Beland R, Carmant L, Lassonde M. Impact of childhood epilepsy on
reading and phonological processing abilities. Epilepsy Behav 2005;7(2):288–96.
[19] Zhao F, Kang H, You L, Rastogi P, Venkatesh D, Chandra M. Neuropsychological
deficits in temporal lobe epilepsy: a comprehensive review. Ann Indian Acad Neurol
2014;17(4):374. -38.
[20] Rizvi S, Hernandez-Ronquillo L, Moien-Afshari F, Hunter G, Waterhouse K, Dash D,
et al. Evaluating the single seizure clinic model: findings from a Canadian center. J
Neurol Sci 2016;367:203–10.
[21] Barnard C, Wirrell E. Does status epilepticus in children cause developmental de-
terioration and exacerbation of epilepsy? J Child Neurol 1999;14(12):787–94.
[22] Karrash M, Tiitta P, Hermann B, Joutsa J, Shinnar S, Rinne J, et al. Cognitive
outcome in childhood-onset epilepsy: a five-decade prospective cohort study. J Int
Neuropsychol Soc 2017;23:332–40.
[23] Weiss EF, Masur D, Shinnar S, Hesdorffer DC, Hinton VJ, Bonner M, Rinaldi J, Van
de Water V, Culbert J, Shinnar RC, Seinfeld S, Gallentine W, Nordli DR, Frank LM,
Epstein L, Moshé SL, Sun S. Cognitive functioning one month and one year fol-
lowing febrile status epilepticus. Epilepsy Behav 2016;64:283–8.
[24] Teutonico F, Mai R, Veggiotti P, Francione S, Tassi L, Borrelli P, Balottin U, LoRusso
G. Epilepsy surgery in children: evaluation of seizure outcome and predictive ele-
ments. Epilepsia 2013;54:70–6.
[25] Lamberink HJ, Otte WM, Geerts AT, Pavlovic M, Ramos-Lizana J, Marson AG,
Overweg J, Sauma L, Specchio LM, Tennison M, Cardoso TMO, Shinnar S, Schmidt
D, Geleijns K, Braun KPJ. Individualised prediction model of seizure recurrence and
long-term outcomes after withdrawal of antiepileptic drugs in seizure-free patients:
a systematic review and individual participant data meta-analysis. Lancet Neurol
2017;16(7):523–31.
[26] Kozyrskyi AL, Prasad AN. The burden of seizures in Manitoba children: a popula-
tion-based study. Canad J Neurol Sci 2004;31(1):48–52.
[27] Russ S, Garro N, Halfon N. Meeting children’s basic health needs: from patchwork to
tapestry. Child Youth Serv Rev 2010;32:1149–64.