Genizi et al.

The Journal of Headache and Pain (2016) 17:42

DOI 10.1186/s10194-016-0625-x
The Journal of Headache
and Pain

RESEARCH ARTICLE Open Access

Pediatric mixed headache -The relationship

between migraine, tension-type headache
and learning disabilities - in a clinic-based
sample
Jacob Genizi1,2,5*, Amal Khourieh Matar1, Mitchell Schertz3, Nathanel Zelnik4,5 and Isaac Srugo1,5

Abstract
Background: Headache is a common complaint among children. The most common primary headache syndromes
in childhood are migraine and TTH. However many times they seem to overlap. The purpose of our study was to
assess the relationship between pediatric migraine, tension-type headache (TTH) and learning disabilities.
Methods: Children presenting with headache to three pediatric neurology clinics in the last 5 years were assessed.
Two hundred sixty-two children, 5–18 years of age, who met the criteria for migraine were included.
Results: Of 262 children (54 % female) who had migraine, 26.2 % had migraine with aura. 59 children (22.5 % of the
full sample) reported also having headaches that met the criteria for episodic TTH/mixed headaches. Females were
more than 2.8 times more likely to experience mixed headaches than males (OR: 2.81, 95 % CI: 1.43–5.54; p <.003).
Multiple logistic regression analysis revealed that older age (p <0.02), family history of aura (p <.02), and (lack of)
TTH (p <.003) were significant predictors of aura, whereas gender was not significant (p >0.20). Children who had
migraine with aura were less likely to have mixed headaches than children who did not have aura (OR: 0.26, 95 %
CI: 0.11–0.63; p <.003). Children with mixed headaches were 2.7 times more likely to have a learning disability
than children with migraine alone.
Conclusions: Episodic TTH and migraine without aura (mixed headaches) in children might be part of a continuum,
which can explain the high incidence of their co-occurrence as opposed to migraine with aura. Children with mixed
headaches have a higher incidence of learning disability compare to those with migraine alone.
Keywords: Migraine, TTH, Children, Epidemiology

Background the symptoms reported as children age is a complicating

Migraine and tension-type headache (TTH) are by far the issue for differential diagnosis which supports the con-
most common types of headache in children [1]. The tinuum model [8–10]. Battistella [4] reported that in 14 %
prevalence of migraine increases from 3 % in the pre- of young children diagnosed as having migraine without
school years to 4–11 % by the elementary school years, aura, symptoms evolved in adolescence to those of
and up to 8–23 % during the high-school years [2]. The episodic tension-type headache. Nachit-Ouinekh [11] also
prevalence of TTH is 9.8–18 % [3–5]. The relationship be- reported instability in the formal assignment of a migraine
tween migraine and TTH is debated. The ICHD-II and III headache and TTH diagnosis and a drift between head-
beta criteria [6, 7] differentiate between the two, viewing ache types. In daily practice, migraine and TTH share
them as wholly different syndromes. However, changes in common epidemiological and clinical features which make
it difficult to differentiate between them. Indeed some
* Correspondence: [email protected]
practitioners claim that the majority of migraineurs also
1
Department of Pediatrics, Bnai Zion Medical Center, Haifa, Israel have TTH [4].
2
Pediatric Neurology Unit, Bnai Zion Medical Center, Haifa, Israel
Full list of author information is available at the end of the article

© 2016 Genizi et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
Genizi et al. The Journal of Headache and Pain (2016) 17:42 Page 2 of 4

The aim of the present study was to assess the preva- Table 1 Demographic and clinical data (number and % or
lence and features of children presenting with simultan- mean ± SD) of children with Migraine
eous migraine and TTH and the association of learning Aura (N = 68) No Aura (N = 192) p
disabilities as a trigger. Gender .01
Male 23 (18.9 %) 99 (81.1 %)
Method Female 45 (32.6 %) 93 (67.4 %)
Study population and design
Age (range) 13.1 ± 2.9 (5–18) 11.5 ± 3.2 (3–21) <.001
We retrospectively reviewed medical records of children
and adolescents who were referred by their primary
physician for neurological assessment due to headaches to times as likely to experience mixed headaches compared
the outpatient pediatric neurology clinics at the Bnai Zion to males (OR: 2.81, 95 % CI: 1.43–5.54; p <.003).
Medical Center, Carmel Medical Center and Meuhedet
Medical Services, all in the city of Haifa, during the years Mixed headaches and migraine with aura
2009–2014. Children and adolescents aged 5–18 years Multiple logistic regression analysis revealed that older
meeting diagnostic criteria for migraine according to age (p <0.02), family history of aura (p <.02) and (lack of)
the 2004 ICHD-II (IHS-2) were included [6]. Children TTH (p <.003) were significant predictors of aura. Gender
with chronic headache were excluded. During their was not significant (p >0.20). Children who had mixed
initial and follow-up visits to the pediatric neurology headaches were 83 % less likely to experience migraine
clinic, all patients and parents were interviewed using with aura than children without mixed headaches (OR:
a semi-structured format according to the HIS criteria 0.17, 95 % CI: 0.05–0.54; p <.003). Conversely, children
and were asked to complete a written questionnaire who had migraine with aura were 74 % less likely to have
and to write a headache diary. Both the interview the mixed headaches than children who did not have aura
questionnaire and the headache diary included questions (OR: 0.26, 95 % CI: 0.11–0.63; p <.003) (Table 2). There
regarding demographics, the patient’s and family’s medical was no association between family history of migraine
history, and headache history (age at onset, location, or age and mixed headaches.
quality, frequency, duration of episodes, aura, and asso-
ciated symptoms). Children who complained of learn-
ing difficulties were given a formal psycho-educational Mixed headaches and learning disabilities
assessment. The study was approved by the Bnai Zion We found a significant association between learning dis-
IRB # 89/14. abilities, diagnosed using a formal psycho-educational
assessment, and mixed headaches (p <.003) (Table 3).
Statistical evaluation Children with mixed headaches were nearly 2.7 times
Comparisons were performed via chi-square tests or Fish- more likely to have a learning disability than children with
er’s exact test where appropriate for the categorical data migraine alone (OR: 2.69, 95 % CI: 1.37–5.28, p <0.003).
and via independent t-tests for the continuous variables.
Odds ratios and their 95 % confidence intervals were com- Discussion
puted. Significance was considered to be p <0.05. Multiple We report on the characteristics of a large cohort of chil-
logistic regression analysis was performed using gender, dren and adolescents with migraine. Our cohort included
age and family history of migraine as main effects. Follow- more females (54 %), and a sizable percentage of children
ing this, stepwise logistic regression was used to evaluate (26 %) experienced aura. These findings are in line with
two-way interactions as potential predictors. Statistical previous reports [12, 13]. The children were asked if they
analysis was performed using SPSS software version 21 experienced additional headaches besides those compat-
(SPSS, Chicago, IL). The study was approved by the local ible with migraine, and 24 % reported having headaches
Helsinki committee. that fulfil the criteria for episodic TTH. Among the group
reporting mixed headaches, the percentage of females was
Results even higher (73 %).
During the study period, 262 children (mean age 12 years,
SD = 2.9) were diagnosed with migraine headache. Of the Table 2 The relationship between TTH headaches and Migraine
total, 138 were female (54 %) and 124 were male (46 %). with Aura
Sixty-eight children (26.2 %) experienced aura (Table 1). TTH (N = 59) No TTH (N = 182) p
Careful history revealed that 59 children (22.5 %) met the Migraine with Aura .03
criteria for episodic TTH/mixed headaches in addition to Yes 10 (14.9 %) 57 (28.2 %)
their migraine headaches; of these, 43 (73 %) were female
No 49 (85.1 %) 125 (71.8 %)
and 16 (27 %) were male. Females were more than 2.8
Genizi et al. The Journal of Headache and Pain (2016) 17:42 Page 3 of 4

Table 3 The relationship between mixed headaches and learning greater comorbidity of migraine and TTH, which is also
disabilities triggered by stress. In males, only a small number should
Migraine have mixed headaches, as most migraines in this group will
TTH (N = 59) No TTH (N = 182) p be caused by something other than stress.
Learning disabilities .003 In our study we found that children with mixed head-
Yes 26 (52.0 %) 37 (28.7 %)
aches were less likely to have migraine with aura. Given
that it is easier to differentiate between migraine with
No 24 (48.0 %) 92 (71.3 %)
aura and TTH, this finding may simply reflect misdiag-
Unknown 9 (15.2 %) 53 (29.1 %) nosis of TTH as migraine without aura. Alternatively, it
may be that TTH is related to migraine without aura
The 22 % overlap between TTH and migraine observed and both are part of a continuum, while migraine with
in our study should be considered against the backdrop of aura is a different disease. This theory is bolstered by
previous studies. Both Silberstein [14] among adults and our findings that the predictors of migraine with aura in-
Viswanathan [8] in children considered migraine and clude family history of aura but not of migraine alone,
TTH to be closely related entities which diverge only and an absence of TTH.
in severity. In support of this argument, a number of Finally, the connection between mixed headaches and
studies among adults (the Spectrum study [15]) and chil- learning disabilities is worthy of mention. In our previ-
dren [16, 17] found an evolution to migraine headache ous study [13] we found that learning disabilities were
among patients with TTH. Turkdogan found that 58 % of more common among children with migraine compared
children with migraine reported TTH features and 68 % to children with TTH alone. D’Andrea [20] and Waldie
of children with episodic TTH had migraine-type features; [21] reported impairment in memory in children with
however, he considered this an overlap between features migraine, with normal performance in reading, motor
of migraine and TTH and vice versa, rather than a syn- and spatial tasks. Parisi [22] found significant differences
drome combining migraine and TTH [10]. The 24 % over- between the headache (Migraine and TTH) and control
lap of TTH and migraine as was demonstrated in our groups in the mean total intelligence quotient and verbal
study can be explained in few different ways. If we are not intelligence quotient scores, and a negative correlation
willing to agree with Silberstein and Viswanathan that mi- between the total intelligence quotient score and the age
graine and TTH are a continuum, it might be due to at headache onset. Haverkamp [23] found no significant
wrong diagnosis. Battistella reported that 14 % of young difference in sequential and simultaneous information
children diagnosed as migraine without aura had evolved processing when comparing the cognitive performance
in adolescents into episodic tension-type headache. But he of children with migraine to their healthy siblings. Previ-
reported that none of children with TTH evolved into ous studies have found that adolescents with headaches
migraine even without aura?! Another explanation might tend to be highly motivated over-achievers [24].
be the common triggers. Pediatric migraine and TTH are Parisi [22] findings that headache starting at early age
both triggered mainly by stress [5, 18] which might causes more intelligence deficit do not confirm that mi-
explain the stimulus presentation. graine headaches and cognitive impairment both arise in
In this regard, the current findings on gender are the early childhood. It may suggest, however, that early
also worth noting. The increased incidence of all mi- age at onset and a high frequency of headache attacks
graine among females in comparison to males is well are associated with cognitive impairment probably owing
known [3, 18]. Laurell, in her population-based survey, re- to the immaturity of the central nervous system at
ported a higher percentage of females in TTH as well as in young age. Among migraine patients, the involvement of
migraine [3]. Lyngberg, in a large epidemiologic study, re- cognitive function might be also related to cortical areas,
ported a male:female ratio of 1:6 in migraine, but only 1:3 such as the frontal and prefrontal areas, as a result of
in episodic tension-type headache [19]. In our study, the poor sleep [25], and sub-cortical areas, as a result of iron
proportion of females was substantially higher among the accumulation in deep brain nuclei [26]. In children with
mixed-headache group (migraine + TTH) than among TTH, Parisi [22] found that the verbal comprehension
those with only migraine. These findings again raise the subtest score alone was significantly lower than in the
question, are mixed headaches really a different syndrome? control group.
Of course, it is also possible that the answer lies in the However, such studies did not distinguish between mi-
common trigger for migraine and TTH, namely emotional graine with and without aura. In the present study we
stress. More specifically, does stress trigger these condi- found a significant association between learning disabil-
tions, and in particular migraine without aura, equally in ities and mixed headaches, but not migraine with aura.
males and females? If stress is the main trigger of migraine These findings cannot be explained on the grounds that
in females but not in males, we can expect females to have stress at school is a trigger for headaches, because this is
Genizi et al. The Journal of Headache and Pain (2016) 17:42 Page 4 of 4

true for both migraine with and without aura. We regard 9. Wober-Bingol C, Wober C, Karwautz A, Auterith A, Serim M, Zebenholzer K,
our findings, including the high percentage of mixed et al (2004) Clinical features of migraine: a cross-sectional study in patients
aged three to sixty-nine. Cephalalgia 24:12–17
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Ruth Rappaport Faculty of Medicine, Technion, Haifa, Israel. accumulation in deep brain nuclei in migraine: a population- based
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Received: 16 February 2016 Accepted: 7 April 2016

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