Eur J Pediatr. 2013 (Oct); 172 (10): 1349–1356 ~ FULL TEXT
Kim Budelmann, Harry von Piekartz, Toby Hall
University of Applied Science,
Pediatric headache is an increasingly reported phenomenon. Cervicogenic headache (CGH) is a subgroup of headache, but there is limited information about cervical spine physical examination signs in children with CGH. Therefore, a cross-sectional study was designed to investigate cervical spine physical examination signs including active range of motion (ROM), posture determined by the craniovertebral angle (CVA), and upper cervical ROM determined by the flexion-rotation test (FRT) in children aged between 6 and 12 years. An additional purpose was to determine the degree of pain provoked by the FRT.
Thirty children (mean age 120.70 months [SD 15.14]) with features of CGH and 34 (mean age 125.38 months [13.14]) age-matched asymptomatic controls participated in the study. When compared to asymptomatic controls, symptomatic children had a significantly smaller CVA (p < 0.001), significantly less active ROM in all cardinal planes (p < 0.001), and significantly less ROM during the FRT (p < 0.001), especially towards the dominant headache side (p < 0.001).
In addition, symptomatic subjects reported more pain during the FRT (p < 0.001) and there was a significant negative correlation (r = -0.758, p < 0.001) between the range recorded during the FRT towards the dominant headache side and FRT pain intensity score. This study found evidence of impaired function of the upper cervical spine in children with CGH and provides evidence of the clinical utility of the FRT when examining children with CGH.
From the FULL TEXT Article:
Headache is the most frequently reported pain in children , with an even sex distribution up to the age of 12 [2, 25, 28], after which more females than males suffer. [25, 49]
Pediatric headache prevalence rates are 50% during school
years, increasing during adolescence to 80%.  Studies
have shown that children with more severe headache report
lower quality in life, in general , while early onset headache
can be predictive of ongoing problems during adolescence
and adult life [8, 18], indicating the importance of
diagnosis and management.
Cognitive, behavioral, and emotional factors have been
shown to play important roles in generating headache in
children. [4, 33] In addition, physical factors, such as
schoolwork, increased forward head posture, and prolonged
static postures of the head [11, 34, 49], have also been
shown to play a role in triggering headache. Hence, headache
diagnosis is important, particularly for physiotherapists
who have to consider whether physical treatment may be
helpful to alleviate symptoms.
There are numerous structures and disorders capable of
causing headache.  The International Headache Society  has formulated the International Classification of
Headache Disorders (ICHD) to enable differentiation of primary
and secondary headache disorders. One form of secondary
headache is cervicogenic headache (CGH), where pain is
believed to originate from a disorder in the neck.  The
anatomical basis for pain perceived in the head is due to the
convergence of afferent impulses from the upper three cervical
nerve roots with the trigeminal nerve in the trigeminocervical
nucleus. [7, 22] The ICHD  is commonly used to diagnose
headache in adults and relies mainly on subjective descriptors
from the patient.  In pediatric headache, such subjective
differentiation is more difficult [27, 49] and physical signs
become increasingly important to identify CGH.
Physical examination has been shown to be successful in
distinguishing CGH fromother headache forms in adults. 
Physical signs characteristic of CGH in adults include impaired
range of rotation in the upper cervical spine identified
by the flexion–rotation test (FRT) [12, 15, 35, 45], decreased
active range of motion (ROM) [23, 51, 52], increased forward
head posture , upper cervical joint dysfunction , and
impaired cervical muscle function. [21, 22] To date, few
studies have investigated these or other factors in children
who suffer from headache [47, 49]. Published normal values
for active cardinal plane ROM in asymptomatic children
indicate larger ranges than adults [3, 29], thus warning of the
difficulty of using adult values when examining children.
The therapist examining children with purported CGH
requires a good knowledge of the musculoskeletal characteristics
of the cervical spine of asymptomatic children in
order to identify differences and potential impairments.
Recent literature advocates the use of the FRT as a useful
means of identification of impairment of the upper cervical
spine and CGH diagnosis in adults. [14, 16, 17] For this test,
the subject's neck is positioned in end range flexion, which
blocks as much rotational movement as possible in the
cervical spine below and above C1/C2 and helps to identify
dysfunctions in the upper cervical spine. [12, 35] In asymptomatic
adults, normal values for ROM during the FRT are
reported as 38° (36) and 45° (13) to each side, while range is
less than 32° is the positive cutoff value.  However, this
test has not been evaluated in children. Furthermore, no
studies have examined the relationship between ROM of
the upper cervical spine and other measures of musculoskeletal
function of the cervical spine in children with headache.
Specifically, there are no studies that have determined the
relationship between cervical posture and ROM of the upper
cervical spine. Indeed, there is very little information regarding
the presence of impairments of the cervical spine
in pediatric headache, in general, or CGH, in particular.
Therefore, the aim of this study was to investigate active
ROM of the cervical spine, forward head posture identified
by the craniovertebral angle (CVA), and the FRT in asymptomatic
children and children with purported CGH in order
to detect possible differences between groups.
A cross-sectional study was designed to assess active ROMof
the cervical spine, the CVA, and the FRT in 30 children with
purported CGH and 34 age-matched asymptomatic children.
Due to logistical reasons, asymptomatic subjects were recruited
from a high school and handball club in Bremen/Germany,
whereas the subjects with purported CGH were recruited from
three physiotherapy departments in the Netherlands. One examiner
lived in the Netherlands and had contact with three
physiotherapy departments that treat children, whereas the second
examiner lived in Germany. This approach allowed a more
practical recruitment of a higher number of feasible subjects.
All children were recruited after consultation and after written
informed consent was provided by their parents. All potential
subjects had been informed of their right to refuse to participate
in the study or to withdraw consent to participate at any time
without reprisal. In addition, the rights of the children were
protected at all times. Thus, the protocol for this study followed
the ethical principles of the Declaration of Helsinki of theWorld
To be included in the asymptomatic group, volunteers
were required to be asymptomatic and between the ages 6
and 12 years. Subjects were excluded if they had headache
more than once per month, any history of cervical spine
surgery, a diagnosis of Down's syndrome or rheumatoid
arthritis, and inability to tolerate the FRT.
Symptomatic children were interviewed and included in
the purported CGH group if they met the inclusion criteria
based on the description outlined by Antonaci et al.  All
children were required to fulfill all five criteria derived from
the original diagnostic criteria for CGH proposed by Sjaastad
et al. , thus indicating “probable” CGH (Table 1). To be
included in the symptomatic group, the children had to have
unilateral or side-dominant headache without side shift ,
associated neck pain or stiffness [6, 43], headache precipitated
by neck movement or postures , headache frequency of at
least an average of one per week, and history of episodic
semicontinuous or continuous headache for at least the previous
3 months. Previous studies [12, 15] have used these
criteria and showed differences in FRT ROM values between
symptomatic and asymptomatic groups of adults.
Potential subjects with CGH were put forward by the
physiotherapy clinics for potential recruitment and the subjects
were then interviewed by one of the examiners. In
total, 46 children were interviewed and of these, 30 children
were found to be suitable for inclusion in the study.
Consequently, 16 children did not meet the inclusion criteria
and were not assessed.
The Keno®-cervical measurement instrument (Kuntoväline
Oy & David Fitness & Medical Ltd., Helsinki, Finland) was
used to measure cardinal plane active cervical ROM during
flexion, extension, lateral bending, and rotation. The Keno®-
cervical measurement helmet (Figure 1) consists of a plastic
frame with two adjustable gravity goniometers, a compass,
and two spirit levels attached to the frame. A previous study
has found a standard error of measurement (SEM) of at most
4°  for a similar measurement device for measuring cervical
ROM. Intrarater reliability has been reported as good,
with intraclass correlation coefficient's [ICC] of 0.64–0.90 , while interrater reliability ICC's range from 0.61 to
The photometry program designed by the Cranio Facial
Therapy Academy (CRAFTA) was used to determine the
CVA from a digital photograph (Figure 2). The CVA is the
angle formed by a horizontal line drawn through the spinous
process of the seventh cervical vertebra (C7) and a line
joining the spinous process of C7 vertebra with the tragus
of the ear. [38, 46] This measurement has shown to be a
reliable indicator for identifying head and neck posture (ICC
0.84) and has a minimal detectable change of 3.6°. [26, 50]
A compass goniometer fixed to the subject's head with
elasticated Velcro straps was used to measure ROM during
the FRT (Plastimo Airguide, Inc. (compasses), 1110 Lake
Cook Road, Buffalo Groove, IL 60089, USA) (Figure 3)
according to a previously reported method.  This measurement
method has been shown to be reliable, even when
used by inexperienced examiners.  Intrarater reliability
is reported as 0.95 (95% CI: 0.90–0.98)  and 0.93
(95% CI: 0.87–0.96) , while the SEM is at most 1.0°
. Range was recorded to the left and right and separately
towards the dominant and nondominant headache sides.
Pain responses associated with the FRT were assessed
with the colored analog scale (CAS). This scale has a
colored triangle on the front with gradations in length and
color, which helps children to estimate their pain intensity,
whereas the reverse side shows numerical ratings between
0 and 10. The CAS has been found to be an accurate and
valid measuring instrument for measuring pain in children
5 years and older. 
Prior to the main study, an interrater reliability study was
conducted. Two examiners, physiotherapists with more than
4 years experience, carried out all tests, one for the asymptomatic
group and one for the group with purported CGH.
To determine interrater reliability, eight volunteers were
tested according to the examination procedure by each examiner.
Subjects were examined independently, with each examiner blind to the other's measured values. Subjects
were tested 5 min apart.
In the main study, all measurements were assessed in a
standardized manner to ensure reproducibility. The CVA was
determined first. Before the subject's photograph was taken,
the camera was fixed to a tripod set 2 m from the subject. The
tripod was equipped with two spirit levels to ensure horizontal
alignment of the camera. The photographed image section
included the lateral view of the head and shoulder girdle down
to the insertion of the deltoid muscle. Each child was barefoot
and asked to stand comfortably in a relaxed stance on a 70-
cm-long and 30-cm-wide piece of carpet.
Following this, each child was given a practical demonstration
of the assessment procedure for all six active ROM
tests. They were also given a trial practice run to warrant
familiarity with the testing protocol. Each child was instructed
to sit with their trunk stationary in an erect posture on a plinth,
with the arms relaxed at their sides. If necessary, the movement
was corrected by the examiner to ensure movement of
the head in only one plane. The child was asked to move their
head to the maximum comfortable range. Following each
movement, subjects were asked to return to the starting position.
Each cardinal plane movement was performed only once.
Subsequently, the FRT was performed while the child was
positioned in supine. This procedure was based on the description
of Hall and Robinson  and Hall et al.  Each
child lay supine on an examination table with their hands
relaxing on their abdomen with the neck passively placed in
end-range flexion. In this position, the head was rotated to
each side to the maximum comfortable range until the examiner
noticed firm resistance or the child requested the movement
to be stopped because of pain. In all cases, resistance
rather than pain limited the movement. Immediately following
the FRT, each child was asked to rate the discomfort felt
during the FRT on the CAS.
All data were analyzed using Statistical Package for Social
Sciences version IBM SPSS Statistics 19. In all cases, alpha
was set at the 0.05 level. Interrater reliability was determined
by an average measure intraclass correlation coefficient
(ICC). The Shapiro–Wilk's test was used to determine
normality of data distribution. Data was analyzed using an
unpaired t test or Mann–Whitney U test to compare mean
values. An unpaired t test was used for normally distributed
data and the Mann–Whitney U test used when this was not
the case. Spearman's rank correlation was used to determine
the relationship between ROM on the FRT and pain
recorded by the CAS as well as ROM on the FRT and the
CVA. The purpose of this analysis was to identify any
possible relationship between impairment measures in children
with purported CGH.
Interrater reliability for ROM recorded during the FRT was
high with an ICC of 0.93 (95% CI: 0.69–0.99) and moderate
to high for the CVAwith an ICC of 0.88 (95% CI: 0.51–
0.97), indicating at least good reliability for these measures.
The asymptomatic group consisted of 34 children (26 females;
mean age 125.38 months [SD 13.14]), whereas the
group with purported CGH consisted of 30 children with a
mean duration of symptoms of 20.7 months (19 females;
mean age 120.70 months [SD 15.14]). An unpaired t test
revealed no significant difference for age between groups
(p=0.58). In the symptomatic group, headache was more
frequently reported as dominant on the right side (19/30,
63.3%) compared to the left (11/30, 36.7%). Means,
standard deviations (SD), ranges in degrees and level of
significance of the variables age, CVA, pain intensity, and
cervical movements are outlined in Table 2.
The CVA of the asymptomatic children and symptomatic
children were 51.26° (SD 4.78) and 47.27° (SD 2.36),
respectively. An unpaired t test revealed a significant difference
of 3.99° in CVA between groups (p<0.001).Similarly,
a Mann–Whitney U test revealed a significant difference
between groups for each active cervical ROM (p<0.001).
The asymptomatic subjects had significantly greater
ROM, as well as cardinal plane ROM differences, recorded
during the FRT to the right and left when compared to the
symptomatic children (p<0.001). Mean ranges of rotation to
the right (52.97/SD 4.65) and left (52.38/SD5.47) were not
significantly different within the asymptomatic group (p=
0.370). However, ranges recorded during the FRT to the
right (34.53/SD 8.11) and left (42.63/SD 7.91) differed
significantly within the symptomatic group (p<0.01).
Furthermore, ROM recorded during the FRT towards the
dominant headache side (33.36/SD 6.57) was significantly
less than the nondominant headache side (43.80/SD 7.93)
The asymptomatic children had no significant increase in
pain (p=0.378) as a result of performing the FRT. However,
this was not the case in the symptomatic group, where subjects
showed a significant increase in pain (p<0.001) after
applying the FRT. Pain intensity scores are shown in
Table 2. The higher pain intensities recorded during the
FRT to the right in the symptomatic group may be due to
the higher prevalence of right-sided headache in this group
(19/30, 63.3% had right-sided headache).
A Spearman's rank correlation was used to determine the
relationship between ROM on the FRT and pain recorded by
the CAS. This analysis revealed a highly significant negative
correlation between the range recorded during the FRT
towards the dominant headache side and the post-FRT pain
intensity score (r=–0.758, p<0.001) with r2 value of 0.574,
indicating that 57.4% of the variance of FRT ROM towards
the dominant headache side is explained by variability in the
CAS pain score. Generally speaking, the lower the ROM
towards the dominant headache side, the higher the post-
FRT pain intensity score.
In addition, the relationship was sought between combined
left and right ROM recorded during the FRT and the
CVA. This analysis revealed a significant positive correlation
(r=0.421, p<0.05) with a r2 value of 0.177, indicating
that only 17.7% of the variance of combined FRT ROM is
predicted by variability in the CVA.
The results of this study show significant differences in all
variables, despite no difference in age and similarity in
distribution of gender. Previous reports indicated a higher
prevalence of headache in girls [24, 25, 49], which is
reflected in our sample of children with headache who were
Cervical range of motion (ROM) in each cardinal plane
was significantly less in the children with purported
cervicogenic headache (CGH) compared to those without
headache (Table 1). ROM values recorded in the asymptomatic
group are comparable with a previous report for children.  While no previous studies have reported ROM
values for children with CGH, these results are consistent
with reports in adult populations. [23, 51, 52] Interestingly,
ROM does not appear to be restricted in all directions in
adults with headache [23, 51, 52], but the explanation for
this is not clear. This study finding of reduced ROM in
children with purported CGH supports the current criteria
for CGH diagnosis. [20, 44]
In addition to differences in ROM, our study found children
with purported CGH had significantly different posture
to asymptomatic children as identified by the craniovertebral
angle (CVA). Children with purported CGH had a significantly
smaller CVA and, therefore, increased forward head posture
when compared with asymptomatic children (Table 1). The
mean CVA of the asymptomatic group is comparable to a
previous report of 55° (SD 9.02) in children whose mean age
was 12 years.  The difference between groups was 4°,
more than the minimal detectable change of 3.6° for this
measurement method.  This finding is consistent with
one previous report in adults with headache  and neck
pain , but in contrast to other reports, which found no
difference in posture between people with and without headache. [9, 51] Previously, only one study has investigated the
CVA in symptomatic children and those with neck pain and/or
headache.  In that study, no difference was found in CVA
between 52 adolescents with pain and 75 adolescents without
pain. Taken as a whole, itwould appear that postural change in
subjects with purported CGH remains equivocal and further
research is required in this area.
To our knowledge, this is the first study investigating the
flexion–rotation test (FRT) in children with purported CGH.
The results revealed three interesting aspects for discussion.
Firstly, the mean range recorded during the FRT in the
asymptomatic group was approximately 8° more than that
reported for asymptomatic adults.  Secondly, the symptomatic
group had significantly less range when compared
to the asymptomatic group. The difference in mean range
recorded towards the dominant headache side and the range
in asymptomatic children was 19°. Lastly, ranges recorded
to the right and left were dissimilar in range in children with
headache, with approximately 8° difference between sides.
One explanation for this could be that of the 30 children
with headache, 19 children reported right-side dominant
symptoms, while only 11 reported the left side as dominant.
Data for ROM towards the dominant and nondominant
headache sides was very similar to range to the left and
the right. The mean difference of 19°, between children with
and without headache, further highlights the usefulness of
the FRT in CGH diagnosis. However, it is important to
recognize that previous reports of a positive cutoff point of
32–33° reported for the FRT in adults [17, 35] should not be
used in children because of their greater mobility. Further
studies are required to identify the positive cutoff value in
It is unclear as to why cardinal plane movement as well as
movement during the FRT is altered in children with purported
CGH. It is clear that degeneration of the cervical spine is
not a factor in this age group. An alternative explanation may
be the presence of altered muscle activation in the cervical
spine associatedwith CGH[26, 51] A recent study  found
massage of the cervical muscles immediately improved range
of motion recorded during the FRT in adults. Similarly, a
Mulligan mobilization with movement technique also gained
immediate range recorded by the FRT.  Interestingly, we
found a strong negative correlation between range recorded
towards the dominant headache side and the pain intensity
scores recorded after the FRT (r=–0.758, p<0.001). In adults,
the presence of headache pain at the time of testing and the
presence of subclinical pain significantly influences the range
recorded during the FRT. [16, 45] Hence, pain and associated
muscle activity may be important limiting factors influencing
upper cervical mobility and the FRT.
In addition to the correlation between the ROM recorded
during the FRTand pain intensity scores, we found amoderate
positive correlation between the ROM recorded during the
FRT and the CVA (r=0.421, p<0.05). This indicates that a
relatively small proportion of the FRT ROM could be
explained by the CVA. One explanation could be the starting
position of the FRT. In contrast to increased forward head
posture where the upper cervical segments are positioned in
extension, the FRT puts the upper cervical spine into full
flexion (13). Consequently, altered head posture and reduced
ROMof the upper cervical spine do not appear to be related in
children with purported CGH. This finding is consistent with
that of adults , which found ROM recorded during the
FRT was only weakly associated with forward head posture.
To our knowledge, this is the first study to investigate
pain provocation during the FRT. Pain levels after the FRT
in the asymptomatic group were very low with a maximum
of 2/10 on the CAS. In contrast, following the FRT, pain
levels were much higher in the children with headache. This
difference may be explained by chronically altered tissue
sensitivity in the children with headache who had a mean
history of headache for 20.7 months.
We acknowledge a number of limitations of this study.
Firstly, a different examiner was used to examine each
group. This was done for logistical reasons with children
with headache all recruited from physiotherapy practices
in the Netherlands, while asymptomatic children were
recruited from Germany. This meant that examiners were
not blind to the subject's group allocation, but they were
trained in the measurement methods. Previously, it has been
reported that when using the FRT, even inexperienced examiners
have good reliability when compared with experienced
examiners.  Secondly, the majority of the asymptomatic
children were recruited from a sports club. Each
child has a different pain perception depending on the personality,
learning, expectations, and previous pain experiences. [30, 31] Consequently, active children who play sport
may have different range of motion, posture, and responses
to testing than less active children.
This study found evidence of impaired function of the
cervical spine in children with purported CGH. When compared
with an asymptomatic group of children, those with
headache had significantly reduced active ROM in all directions,
significantly less range recorded during the FRT,
significantly higher pain scores following the FRT, and
significantly greater forward head posture. This information
may be useful to clinicians in the identification of children
with suspected CGH. Decreased ROM and pain provocation
during the FRT appears to have potential diagnostic value.
This study sets the groundwork for future studies investigating
headache in children. Future studies should investigate
the diagnostic value of these tests in the identification
of CGH from other headache forms such as migraine or
tension-type headache. In addition, impairments of the cervical
spine as a contributing factor to different pediatric
headache forms needs to be clarified in more detail.
Conflicts of interest
CAS = Colored analog scale
CGH = Cervicogenic headache
CI = Confidence interval
CVA = Craniovertebral angle
FRT = Flexion rotation test
ICC = Intraclass correlation coefficient
ROM = Range of motion
SD = Standard deviation
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