Features of migraine aura in teenagers

Abstract

Complex migraine aura in teenagers can be complicated to diagnose. The aim of this study was to present detailed features of migraine aura in teenage migraineurs.
This cross-sectional study was conducted in the period from 2008 till 2013. A total number of 40 teenage migraineurs (20 females and 20 males) met criteria for this study. The patients were interviewed using a specially designed questionnaire for collecting data about migraine aura features. Main outcome measures were frequency of visual, somatosensory and higher cortical dysfunction (HCD) symptoms in teenage migraineurs population during the aura, and also within each individual.
Visual aura was reported in every attack, followed by somatosensory (60%) and dysphasic (36.4%) aura. Scintillating scotoma and blurry vision were mostly reported and predominant visual symptoms. The most common somatosensory symptom was numbness in hand. HCD were reported by 22 (55%) patients. Slowed speech was mostly reported symptom of HCD, followed by dyslexia, deja vu phenomenon, color dysgnosia, and dyspraxia. In patients with HCD, aura frequency per year (6.18 +/- 3.17 vs. 3.33 +/- 2.03, p = 0.003) and prevalence of somatosensory symptoms (77.3% vs. 38.9%, p = 0.014) were significantly higher than in patients without HCD.
Aura symptoms vary to a great extent in complexity in teenage migraineurs. Consequently, results obtained in this study provide useful information for clinicians when faced with unusual migraine aura.

Full text

R E S E A R C H A R T I C L E Open Access
Features of migraine aura in teenagers
Igor Petrusic
2*
, Vera Pavlovski
2
, Dragana Vucinic
1
and Jasna Jancic
1,2
Abstract
Background: Complex migraine aura in teenagers can be complicated to diagnose. The aim of this study was to
present detailed features of migraine aura in teenage migraineurs.
Methods: This cross-sectional study was conducted in the period from 2008 till 2013. A total number of 40 teenage
migraineurs (20 females and 20 males) met criteria for this study. The patients were interviewed using a specially
designed questionnaire for collecting data about migraine aura features. Main outcome measures were frequency
of visual, somatosensory and higher cortical dysfunction (HCD) symptoms in teenage migraineurs population during
the aura, and also within each individual.
Results: Visual aura was reported in every attack, followed by somatosensory (60%) and dysphasic (36.4%) aura.
Scintillating scotoma and blurry vision were mostly reported and predominant visual symptoms. The most common
somatosensory symptom was numbness in hand. HCD were reported by 22 (55%) patients. Slowed speech was
mostly reported symptom of HCD, followed by dyslexia, déjà vu phenomenon, color dysgnosia, and dyspraxia. In
patients with HCD, aura frequency per year (6.18 ± 3.17 vs. 3.33 ± 2.03, p = 0.003) and prevalence of somatosensory
symptoms (77.3% vs. 38.9%, p = 0.014) were significantly higher than in patients without HCD.
Conclusions: Aura symptoms vary to a great extent in complexity in teenage migraineurs. Consequently, results
obtained in this study provide useful information for clinicians when faced with unusual migraine aura.
Keywords: Migraine aura; Higher cortical dysfunction; Teenagers
Background
The estimated overall mean prevalence of migraine in
children and adolescents worldwide was 7-11% [1].
Thereof, 25% of patients with migraine experience an
aura [2]. Migraine aura is commonly considered to pre-
cede headache [3]. Visual auras are the most common,
followed by somatosensory, and then dysphasic auras [4].
Motor aura is the least common and is a defining feature
of hemiplegic migraine [5].
Migraine aura is thought to arise due to a change in
cortical neural excitability and function [6]. Cortical
spreading depolarization followed by cortical spreading
depression (CSD), mostly originates in the occipital
region [7]. The involvement of other cortical areas
beyond the occipital region could be assumed because
of the existence of somatosensory and memory clinical
features during the aura in some patients [8,9].
Diagnosis of migraine in the developmental age is
more difficult and associated with imprecise description
of the symptoms. Moreover, acute confusional migraine
is primarily seen in children and adolescents [10]. The
confusional state often manifests with a wide diversity of
cortical dysfunctions, such as speech difficulties, amnesia,
dysgnosia and dyspraxia [11]. Knowledge of migraine aura
symptoms, clinical differences associated with develop-
mental age and features are very important in differenti-
ation with other disorders imitating migraine [12].
This study represents an attempt to present detailed
features of migraine aura in teenagers. Furthermore, the
aim of this study was to evaluate the frequency and
types of higher cortical dysfunctions (HCD) that occur
during the aura.
Methods
Total of 67 teenagers having migraine with aura, treated
from the beginning of 2008 to the end of 2013 (six years),
at the Clinic of Neurology and Psychiatry for Children and
Youth, Medical Faculty, University of Belgrade, were
called to participate in this study. The diagnosis was based
* Correspondence: ip7med@yahoo.com
2
Faculty of Medicine, University of Belgrade, Doktora Subotica 8, 11000
Belgrade, Serbia
Full list of author information is available at the end of the article
© 2014 Petrusic et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction
in any medium, provided the original work is properly credited.
Petrusic et al. The Journal of Headache and Pain 2014, 15:87
http://www.thejournalofheadacheandpain.com/content/15/1/87

on the International Classification of Headache Disorders
criteria [13]. Excluding criteria were: other neurological
diseases, motor aura symptoms [13], chronic migraine
and patients who did not respond to a call. Forty patients
who met inclusion criteria have accepted to participate in
this study. A special questionnaire (Table 1) was designed
to collect data on migraine aura features and HCD during
the aura. Positive responses to each question of designed
questionnaire were followed by the sub-questions for the
purpose of collecting information how long this symptom
lasts, when this symptom starts in comparison to begin-
ning of headache, how frequent this symptom is present
in aura (in percentage) and whether symptom develops
gradually. The patients were interviewed by a doctor
(I.P. or V.P.), experienced in headache research. Research
protocol of this study was approved by the review board
of the Clinic of Neurology and Psychiatry for Children
and Youth, Medical Faculty, University of Belgrade.
The data are presented as arithmetic mean values ± SD
or as percentages. For analysis purpose, we formed a
group of patients who experienced one or more HCD
symptoms during the aura (HCD group) and a group of
patients who did not experience HCD (Standard aura
group). Independent samples t test was used to compare
the age of patients and the age at the time of the onset
of migraine with aura; Chi squared test was used to
compare gender, number of patients who reported
somatosensory symptoms in general and who reported
numbness in hand; Fisher's exact test was used to com-
pare the number of patients who reported numbness of
arm, leg, tongue, face and lips; and the Mann–Whitney
U test was used to compare aura duration and the number
of auras per year between the groups. The significance
level for the analysis was set beforehand at 5% (p < 0.05).
Result
The study included 20 females and 20 males, aged
16.2 ± 2.0 (range 13–19) years, who experienced migraine
with aura. Fifteen (37.5%) patients had visual aura only; 10
(25.0%) patients had visual and somatosensory auras; and
15 (37.5%) patients had visual with/or without somatosen-
sory and with dysphasic aura.
Visual and somatosensory symptoms of aura in teenage
migraineurs are described in Table 2. All patients had one
or more visual symptoms. Scintillating scotoma was the
most commonly reported (67.5%) and predominant (94%)
visual symptom during the aura. Somatosensory symp-
toms were less common than visual with occurrence of
60% in patients. Most common was numbness in the left
hand or both hands (2 patients) reported in 21 patients
(52.5%), followed by numbness in: lips and/or face (30%),
tongue (27.5%), and legs (15%). Two patients had acute
onset visual aura, followed by short presentation of
somatosensory symptoms and HCD. Also, two patients
had prolonged visual aura, who reported gradual develop-
ing of somatosensory and dysphasic symptoms. Overall, in
ten patients migraine aura proceeded during headache for
12.6 ± 10.2 (range 3–30) minutes and four patients re-
ported period of 7.5 ± 2.9 (range 5–10) minutes between
migraine aura and onset of headache. Twenty-six patients
reported onset of headache immediately after finish of
aura.
HCD were reported by 22 (55%) patients in this study.
A detailed description of HCD during the aura in teen-
age migraineurs analyzed group (40 patients) was given
in Table 3. The majority of patients with HCD during
the aura reported one, two, or four HCD symptoms, as
shown in Figure 1. Slowed speech was the most usually
reported (27.5%) symptom of HCD during the aura,
followed by dyslexia (25%), déjà vu phenomenon (22.5%),
color dysgnosia (20%), and dyspraxia (20%). Prosopagnosia
was reported in one (2.5%) patient, while difficulties in un-
derstanding speech or recognizing sounds and difficulties
in writing were not reported. Color dysgnosia, slowed
Table 1 Study questionnaire
During the aura of your migraine attack, have you ever noticed:
1. Shimmering or blurred dots in the visual field?
2. Twinkling zig-zag lines in the visual field?
3. Blurred vision (like looking through tick glass)?
4. Tunnel vision (narrowing of the visual field)?
5. Tingling or numbness in fingers, hand, leg, face (lips) and tongue?
6. Changes in colors? Did colors get brighter or paler?
7. Difficulties in recognizing faces, unrelated to the disturbance
of vision?
8. Difficulties in recalling names?
9. Difficulties in recalling events from the past?
10. Difficulties in remembering events during aura?
11. The feeling that you have already seen events (déjà vu
phenomenon)?
12. Difficulties in speaking even when you knew what you wanted
to say?
13. Did someone tell you that you speaking gibberish?
14. It takes more time to find the appropriate words when you try
to speak?
15. Difficulties in understanding speech or recognizing sounds
from the environment?
16. Difficulties in understanding writing, unrelated to visual disorders?
17. Difficulties in writing that were not caused by the disturbance
of vision?
18. Difficulties in calculating and/or memorizing numbers?
19. Difficulties in recognizing objects by touch?
20. Difficulties in performing normal movements with your hands?
21. Difficulties in orientation in space (in terms of left and right)?
22. Unawareness of one part of your body?
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speech and manual dyspraxia were most frequently expe-
rienced symptoms. Moreover, 14 (35%) patients have ex-
perienced one or more HCD symptoms in more than one
third of their auras.
Patients with HCD during aura were classified as HCD
group. The 18 patients who did not experience HCD
during aura were classified as Standard aura group.
Comparison of demographic data and features of aura
between these groups are shown in Table 4. There was
no statistically significant difference in terms of gender,
age at the time of examination, age at migraine onset
and duration of aura. Also, these two groups did not sig-
nificantly differ in number of patients who reported
numbness in arms, face and lips as symptom during the
aura. Frequency of aura per year was significantly higher
in HCD group (6.18 ± 3.17 vs. 3.33 ± 2.03, p = 0.003), as
well as the number of patients with somatosensory
symptoms during aura (77.3% vs. 38.9%, p = 0.014). Also,
HCD group had significantly more patients who reported
numbness in hands, tongue and legs compared to Stand-
ard aura group.
Discussion
These are the first detailed nosographic descriptions, to
our knowledge, of the symptoms experienced during the
aura reported by teenagers who have migraine with aura.
Our data show that neurological non-visual symptoms,
including HCD, during the aura in teenage migraine are
notable. Also, the findings of this study clearly demon-
strate the variability of aura symptoms. To our opinion,
these are important information for pediatricians and
other physicians when facing new cases of migraine with
unusual aura.
The most common manifestation of migraine with aura
is visual phenomenon [14], reported by all our patients.
Besides the simple positive or negative phenomena, high
number of patients have also reported some form of
complex visual disturbances. The most frequent visual
Table 2 Visual and somatosensory symptoms during the aura
Visual and somatosensory
aura features
Number of patients Onset time X ± SD
(min-max)
Time duration
X ± SD (min-max)
Frequency X ± SD
(min-max)
n = 40 (%)
Scintillating scotoma 27 (67.5) 21.24 ± 15.87 (25–60) 18.67 ± 16.62 (2–75) 94.26 ± 17.25 (25–100)
Zig-zag lines 10 (25) 23 ± 12.06 (5–45) 19.5 ± 12.12 (5–45) 90 ± 23.09 (30–100)
Blurry vision 24 (60) 22.22 ± 12.12 (2–45) 19.29 ± 14.53 (2–45) 85 ± 27.54 (10–100)
Tunnel vision 16 (40) 24.69 ± 14.54 (5–60) 18.44 ± 12.48 (5–60) 74.38 ± 35.02 (10–100)
Somatosensory symptoms 24 (60) 22.06 ± 17.3 (2–60) 17.5 ± 16.9 (2–60) 62.5 ± 31.21 (10–100)
Onset time - aura onset in regard to beginning of headache expressed in minutes; Time duration - expressed in minutes; Frequency - frequency of symptom
compared to all experienced auras in individual (expressed in percentages).
Table 3 Features of HCD during the aura reported in teenage migraineurs
HCD Number of patients Onset time X ± SD
(min-max)
Time duration
X ± SD (min-max)
Frequency X ± SD
(min-max)
n = 40 (%)
Color dysgnosia 8 (20) 8.5 ± 6.48 (2–20) 7.13 ± 6.1 (2–20) 60 ± 40.71 (10–100)
Dysnomia 3 (7.5) 15.67 ± 14.01 (2–30) 15.67 ± 14.01 (2–30) 46.67 ± 46.19 (20–100)
Retrograde amnesia 4 (10) 16.75 ± 15.35 (2–30) 16.75 ± 15.35 (2–30) 41.25 ± 21.75 (20–70)
Anterograde amnesia 2 (5) n/a n/a 10
Déjà vu phenomenon 9 (22.5) 20.25 ± 11.17 (2–30) n/a 30.56 ± 14.24 (10–50)
Expressive dysphasia 5 (12.5) 21 ± 15.59 (3–30) 15.6 ± 13.39 (3–30) 47 ± 36.33 (20–100)
Gibberish speaking 2 (5) 16.5 ± 19.09 (3–30) 16.5 ± 19.09 (3–30) 45 ± 35.35 (20–70)
Slowed speech 11 (27,5) 19.75 ± 19.51 (3–60) 18.64 ± 17.44 (2–60) 59.55 ± 39.9 (10–100)
Dyslexia 10 (25) 21.5 ± 944 (10–30) 21.5 ± 17.89 (3–60) 41.5 ± 27.49 (10–100)
Dyscalculia 2 (5) 37.5 ± 31.82 (15–60) 25 ± 28.28 (5–45) 30 ± 28.28 (10–50)
Astereognosis 2 (5) 16.5 ± 19.09 (3–30) 8 ± 9.9 (1–15) 55 ± 63.64 (10–100)
Manual dyspraxia 8 (20) 21.13 ± 20.25 (4–60) 18.75 ± 21.96 (2–60) 46.88 ± 37.51 (10–100)
Right-left confusion 5 (12.5) 18.75 ± 17.97 (5–45) 13.6 ± 17.74 (3–45) 51 ± 45.33 (10–100)
Neglecting hand symptom 2 (5) 17.5 ± 17.68 (5–30) 17.5 ± 17.68 (5–30) 50 ± 28.28 (30–70)
Onset time - aura onset in regard to beginning of headache expressed in minutes; Time duration - expressed in minutes; Frequency - frequency of symptom
compared to all experienced auras (expressed in percentages); n/a - not applicable.
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symptom was scintillating scotoma, followed by blurry
vision, tunnel vision and zig-zag lines. These symptoms
had gradual development which corresponds with typic-
ally described migraine aura [13]. High prevalence of
blurry vision and tunnel vision (shrinking of visual field)
in our patients, not typically considered to be an aura
phenomenon of cortical origin, support recent findings
towards heterogeneous symptoms of visual aura [15].
Moreover, visual dysgnosia during the aura was frequently
reported by our patients in contrast to findings in litera-
ture [16]. Color dysgnosia, in terms of this - colors get
brighter and patients had difficulties in recognition of
color shades, was most commonly reported symptom of
visual types of dysgnosia and most frequently experienced
symptom in patient auras. This could be explained by the
fact that visual auras could arise from the primary visual
cortex, as well as from other extrastriate areas (e.g. V2,
V3yVP, V3A, and V4v) [17,18]. In the other hand,
prosopagnosia was reported in only one patient. This
could be due to the fact that this function is localized
bilaterally [19].
The second most common type of aura in our group
of patients was somatosensory phenomena (60%). The
most frequently reported somatosensory symptom was
Figure 1 Distribution of patients by number of HCF disturbances. HCF: higher cortical function.
Table 4 Comparison of demographic data and aura features between HCD group and standard aura group
Demographic data, aura characteristics HCD group (n = 22) Standard aura group (n = 18) Statistics
Gender –girls (%) 10 (45.5) 10 (55.6) p = 0.525
Age of patients, X ± SD, years 16.32 ± 1.98 16.06 ± 2.1 p = 0.687
Age at the time of the onset of migraine, X ± SD, in years 13.18 ± 1.74 12.17 ± 2.97 p = 0.212
Aura duration, X ± SD, in minutes 30.91 ± 20.85 27.5 ± 10.04 p = 1.000
Number of auras per year, X ± SD 6.18 ± 3.17 3.33 ± 2.03 p = 0.003
Somatosensory symptoms (%) 17 (77.3) 7 (38.9) p = 0.014
Numbness in hands (%) 16 (72.7) 5 (27.8) p = 0.005
Numbness in arms (%) 9 (40.9) 2 (11.1) p = 0.073
Numbness of the face and lips (%) 9 (40.9) 3 (16.7) p = 0.165
Numbness of the tongue (%) 10 (45.5) 1 (5.6) p = 0.011
Numbness in legs (%) 6 (27.3) 0 (0) p =0.024
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numbness in hand (52.5%), while 15% of the patients
reported numbness in legs with “marching”phenomenon,
which is in line with previous similar study in adult popu-
lation with migraine [20]. Interestingly, patients with
visual and somatosensory aura mainly reported 5 to 10
minutes delay of beginning of somatosensory symptoms
after beginning of visual aura, but also in eight patients
somatosensory aura onset occurred at the same time or
before visual aura. These findings could indicate multiple
origin of CSD in some of patients, which is previously
proposed [17,20]. It is noteworthy that all patients had
normal imaging examinations that excluded a structural
lesion which might either account for or be caused by the
hyperexcitability that triggers migraines [21].
Beyond the visual and somatosensory symptoms, phe-
nomena reported during the migraine include mispercep-
tions, impaired gnosis, praxis, and memory [8]. In our
study, HCD during the aura were notable. Slowed speech
and problems in reading as symptoms during the aura
were the most usually reported. Moreover, 36% of teenage
migraineurs had some type of dysphasic disturbances dur-
ing the aura, which is high in comparison to 15% reported
by Russell MB and Olesen J [16], but less than in our pre-
vious study where dysphasic symptoms were reported by
53% of adults with migraine [11]. Furthermore, in teen-
agers with migraine symptoms of expressive dysphasia
were less common (12%) in comparison to adult’smi-
graine [14]. We can only speculate that in teenage
migraineurs CSD rarely reach Broca's region. Also, in
our opinion, it is very important to focus on the diver-
sity of dysphasic presentation among migraineurs in
further investigations.
One of ten of our patients had memory disturbances
during the aura, such as difficulties in remembering the
events or more frequently in recalling past events. In pa-
tients who had these symptoms every second migraine
aura was accompanied by retrograde amnesia. Memory
processes involve regions in the medial temporal lobes
including the hippocampus, which may be implicated
during CSD [8]. Déjà vu phenomenon was reported by
22.5% of our patients, mostly in one third of their auras.
Also, our patients reported difficulties in calculating, nam-
ing, performing precise movements with hands, orienting
in space, recognizing objects by touch, as well as neglecting
hand symptom. Frequency of all these HCD occurrences
point out the variety of possibilities of CSD propagating
through the cortex [8,21].
Further, we compared two subgroups of patients who
experienced one or more HCD symptoms during the
aura (HCD group) and those who did not experienced
HCD (Standard aura group). Main findings were that
these subgroups did not differ in terms of gender, age
of patients, age at the time of the onset of migraine,
aura duration and location of the beginning of visual
disturbances in the visual field. This is in line with
findings in adult migraine population, except for aura
duration, where migraineurs with HCD during the aura
had significantly longer duration of aura [11]. Also,
HCD group has significantly higher number of auras
per year compared to Standard aura group. We can only
speculate that this could be due to networks immaturity
in teenagers with migraine, which is demonstrated in
adolescents [22-24]. Also, we found higher prevalence
of somatosensory symptoms in HCD group compared
to Standard aura group. Furthermore, we can assume
that wideness of somatosensory cortex affected region
and CSD intake of secondary somatosensory regions is
linked to the number and types of HCD, because the
somatosensory cortex plays major importance in mul-
tisensory integration processes [25-27].
It should be also mentioned that we had ten patients
whose migraine aura proceeded after onset of headache
for some period of time. This finding could be of interest
for further investigation and more deeply understanding
of aura features influence on quality of pain.
The main limitations of our study are the facts that
data were collected between attacks and that HCD were
determined by patients’reports. Nevertheless, as the ma-
jority of our patients experienced more than 10 auras with
a monthly appearance of aura, we could suppose that their
descriptions are relevant. Although complex or less
clear cognitive changes are particularly susceptible to
recall biases, the results clearly indicate that certain
cortical dysfunctions must be largely underestimated
in migraine because specific questioning is not part of
the routine clinical evaluation.
Conclusions
The analysis of the present cases and general experience
[8,11,16] indicates that aura symptoms, regardless of their
form, vary to a great extent in duration and complexity
from patient to patient, and also within each individual.
Hence, we have concluded from our nosographic analysis
of migraine aura in teenagers that higher cortical distur-
bances should be examined more profound in patients.
Also, continuously reporting of aura features in teenagers
with migraine with HCD during the aura represent great
opportunity for neuroimaging investigation of CSD impact
on cortex development in adolescents.
Consent
Written informed consent was obtained from the patient’s
parent for the publication of this report.
Competing interests
The authors declare that they have no competing interests.
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Authors’contributions
IP carried out study design, interviews with patients, analysis and
interpretation of data and drafted the manuscript. VP participated in data
collection. DV participated in patient selection and provided database of her
patients. JJ carried out study supervision, provided database of her patients
and revised the manuscript for content. All authors read and approved the
final manuscript.
Disclosure
This work was supported by a grant from the Ministry of Science and
Technology of the Republic of Serbia (project no. 41020).
Assoc. Professor Dr. Jancic has received research grant support by the
Ministry of Education and Science, Republic of Serbia (project no. 175031).
Author details
1
Clinic of Neurology and Psychiatry for Children and Youth, CCS, Doktora
Subotica 6a, 11000 Belgrade, Serbia.
2
Faculty of Medicine, University of
Belgrade, Doktora Subotica 8, 11000 Belgrade, Serbia.
Received: 10 October 2014 Accepted: 7 December 2014
Published: 12 December 2014
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doi:10.1186/1129-2377-15-87
Cite this article as: Petrusic et al.:Features of migraine aura in teenagers.
The Journal of Headache and Pain 2014 15:87.
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