Abstract
Objective: This study aimed to evaluate the presence of pressure-painful scalp arteries in children and adolescents with migraine.
Materials and methods: Pressure-painful points on scalp arteries were searched in 130 consecutive children (6–12 years old) and adolescents (
Results: In the absence of a migraine episode, we examined 76 patients: 54 (71.1%) reported one or more pressure-painful arteries and 22 reported none. Of the 40 controls, pressure-painful arteries were present in 11, with a highly significant difference (p < 0.0001).
During a migraine attack, of the 54 patients examined, 43 (79.6 %) reported one or more pressure-painful arteries and 11 reported none. The arteries most frequently painful were the frontal branch and the superficial temporal artery.
Conclusions: Scalp arteries are frequently painful on pressure in children and adolescents with migraine, both in the absence of and during a migraine attack. Painful arteries suggest hypersensitivity of periarterial nociceptive afferents.
Introduction
The role of intracranial neurovascular structures in migraine has been supported by numerous data, as recently reviewed by Olesen et al. (1). The review by Olesen and colleagues (1) put forward few arguments with regard to the role of extracranial structures. A further argument in favour might be the clinical evidence of the positive effect of injections of onabotulinumtoxinA into the scalp in chronic migraine (2,3). We recently reported data in favour of a role of neurovascular scalp structures in some patients with migraine (4–7). These included the presence of tender points on one or more scalp arteries in adult migraine sufferers (8).
Here we report the results of a study on the presence of scalp arterial tender points in children and adolescents of different ages accompanied by a history of migraine, studied both in the absence of and during migraine attacks, which could provide information on the development and evolution of this hypersensitivity in relation to a history of migraine.
Materials and methods
Subjects
A consecutive series of ambulatory children and adolescents with migraine, according to the International Classification of Headache Disorders, 2nd edition (ICHD-II) criteria (9), were recruited for the study.
We examined 130 patients, 89 females and 41 males, 109 without aura (73 females) and 21 with aura (16 females). Their ages ranged from 6 to 18 years (mean 12.8 ± 3.3 years); 67 (40 females) were 6–12 years old (hereafter to be referred to as ‘children’) and 63 (49 females) were ≥13 years old (hereafter to be referred to as ‘adolescents’). Their history of migraine attacks ranged from 1 year to 10 years (mean 3.2 ± 2.5 years).
Of the 130 patients, 76 (48 females) were examined in the absence of headache (40 children and 36 adolescents) and 54 (41 females) during a migraine attack (27 children and 27 adolescents). As a control, 40 subjects (25 females; 22 children and 18 adolescents), inpatients or outpatients of the department and not suffering from migraine, underwent the same procedures. Their mean age was 11.2 ± 2.9 years. All examined subjects gave written informed consent.
Procedures
According to our protocol for routine examinations of headache patients, each patient was examined to detect pressure-painful points on scalp arteries. We used the same procedures outlined in the Cianchetti et al. study on adults with migraine and followed the protocol described in that study (8). In brief, the examination included the following arteries: the superficial temporal artery, its frontal branch, the zygomatico-orbital artery, and the occipital and posterior auricular arteries, all examined bilaterally. The arteries were located by detecting their pulse with the light pressure of one or more fingertips; compression in order to detect arterial pain was exerted using the same fingertips. Pressure intensity was within an established range that the experienced investigators were well accustomed to using. According to a comparative evaluation with an algometer (Wagner FDN 50 equipped with a 1-cm2 rubberized applicator tip (Wagner Instruments, Greenwich, CT, USA)), we chose an intensity between 1 and 2 kg/cm2 on the temporal, frontal and zygomatico-orbital arteries and an intensity between 1.5 and 2.5 kg/cm2 on the occipital and auricular arteries. This pressure intensity is lower than that employed in other studies of myofascial pressure pain (10–11). For each compressed artery, the subject was asked to rate pain on a four-point scale (0–3) by extending the fingers of a closed hand on the corresponding side during bilateral compression on the homonymous arteries involved.
The main parameters evaluated were: 1) the number of pressure-painful arteries; 2) ‘severity’, a term used to indicate the sum of the degrees of intensity (1–3) found for each painful artery. The study was approved by the local human research committee.
Results
No migraine during examination
Of the 76 patients (mean age 12.4 ± 3.6) examined out of migraine attack, 54 (71.1%; 36 females) reported one or more pressure-painful arteries and 22 (28.9%; 12 females) none. Pressure-painful arteries were present in 64.3% of males and in 75.0% of females.
With regard to age, of the 40 migraine sufferers under the age of 13 (21 males, 19 females; 35 without aura and five with aura), 24 (60.0%) had one or more pressure-painful arteries and 16 had none. Of the 36 adolescents (seven males and 29 females; 26 without aura and 10 with aura) 30 (83.3%) had one or more pressure-painful arteries and six had none, significantly more compared to children (χ2 = 5.02; p = 0.025).
The number of painful arteries in the 54 patients having at least one painful artery was as follows: one artery in seven patients, two arteries in nine patients, three arteries in 11 patients and four or more arteries in 27 patients (in this calculation, when tenderness involved the same artery bilaterally it was counted as two points), with a mean of 3.9 ± 2.1 painful arteries. With regard to severity (the sum of the degrees of intensity for each painful point), the 54 migraine sufferers showed a mean value of 6.0 ± 4.4.
In the 40 controls, only 11 (27.5%; nine females; eight 7–12 years old) presented painful arteries, with a highly significant difference when compared to migraine sufferers (χ2 = 20.2; p < 0.0001). Of the 11, three had two painful arterial points, three had three, and five had four or more painful arterial points, with a mean number of 3.6 ± 1.5 painful arterial points and a mean severity of 4.6 ± 2.9.
Pressure-painful arteries in the absence of migraine in 54 patients (of 76 examined) and during a migraine attack in 43 patients (of 54 examined)
t = superficial temporal artery; f = frontal branch; z = zygomatic; o = occipital; a = auricular (posterior).
In the upper part of each section (i.e. in the absence of migraine and during a migraine attack, respectively), the total number of arteries found to be painful, either monolaterally or bilaterally, is shown (for reasons of space, no distinction has been made in the table between monolateral and bilateral location on the same artery).
In the lower part of each section, the most frequent associations of painful arteries, either monolaterally or bilaterally, in the same patient is shown.
No correlation was found between the number of painful arteries and headache frequency during the last month (r = 0.073, p = 0.59) and the duration of the disorder (r = 0.121, p = 0.38). Correlation was also lacking if we took into account severity versus migraine frequency during the last month (r = 0.145, p = 0.29) and the duration of the disorder (r = 0.101, p = 0.47).
Migraine attack during examination
Of the 54 patients examined during a migraine attack, 43 (79.6%; 33 females) reported one or more pressure-painful arteries and 11 (20.4%; 8 females) reported none. No significant differences were found in relation to sex (females = 80.5%; males = 76.9%). With regard to age, 27 of the 54 patients were <13 years old (children) and 27 were ≥13 years old (adolescents).
Of the 27 children (six males and 21 females), 21 (77.8%; two with aura and 19 without aura) presented one or more pressure-painful arteries and six presented none (none of these had aura). Of the 27 adolescents (seven males and 20 females), 22 (81.5%; four with aura and 18 without) presented one or more pressure-painful arteries and five presented none (none with aura).
Each of the 43 patients (21 children and 22 adolescents) had one or more painful arteries as follows: one painful artery in three patients, two painful arteries in seven, three in four and four or more in 29 patients (when tenderness involved the same artery bilaterally it was counted as two points), with a mean of 4.4 ± 2.4 painful arteries and a mean 7.6 ± 5.1 severity.
The location of tender points is shown in Table 1. As reported in the absence of migraine attack, the frontal, temporal and occipital arteries were the most frequently painful, considered both individually and in association, and arterial pain was not infrequently localized to one or more segments and not to the whole palpable artery.
No correlation was found between the number of painful arteries and migraine frequency during the last month (r = 0.181, p = 0.24) and the duration of the disorder (r = 0.021, p = 0.89). Correlation was also lacking if severity versus migraine frequency in the last month (r = 0.135; p = 0.39) and duration of the disorder (r = 0.004, p = 0.98) were taken into account.
Although children were not always able to locate the spontaneous pain precisely, migraine at the time of arterial examination was prevalently anterior in 28 cases, diffuse in eight, medioposterior in six and hemicranial in one child. Pressure-painful arteries were located in the area of referred spontaneous migraine headache pain in 39 patients (90.7%), 18 children (of 21) and 21 adolescents (of 22).
Discussion
Our study shows that in children and adolescents suffering from migraine, as with adults, scalp arteries are frequently painful on pressure, both in the absence of and during a migraine attack. Like adult patients, more than one artery is frequently painful in the area of spontaneous migraine headache pain and no differences with regard to the presence or absence of aura could be established.
Unlike adults, there is no difference between males and females with regard to the prevalence of tender points (during development migraine is not as prevalent in females as it is in adulthood) and there is better concordance between the site of arterial pain and migraine location.
No other reports on arterial tenderness in children and adolescents suffering from migraine are found in the literature. Many studies have evaluated either the pressure-pain threshold or tenderness or the trigger points in pericranial and neck muscles in migraine. In the only study on children, Anttila et al. (12) found the suboccipital muscle insertion region, a region where the occipital artery could be inadvertently compressed, as being the most sensitive. In adults suffering with migraine, Calandre et al. (10) found the most frequent ‘trigger’ (not only ‘tender’) points located in the same areas (‘anterior temporal’ in 42.6% and ‘suboccipital’ in 33.4%) of the arteries which we also found to be the most frequently painful. Since they did not evaluate whether they were exerting pressure on an artery (no search for pulsation is reported), it is likely that they actually did so without being aware of it. The same might have happened for at least part of the frontal and anterior temporal tender points tested by Fernández-de-las-Peñas et al. (11).
Our data suggest that arterial pain is inherent in migraine, while attack frequency and duration of the disorder are regulated by other factors, such as the hypersensitivity of the centres that regulate pain.
Painful arteries suggest hypersensitivity of periarterial nociceptive afferents, perhaps due to the local presence of endogenous algogenic products. Dilution of these products could explain the effect of periarterial injection of simple saline (8). Alternatively, a local hypersensitivity of pain receptors located in the periarterial afferent fibres might be involved. This fits in with the beneficial effect of the injection of a local anesthetic (6) and the topical administration of capsaicin cream (13).
Footnotes
Acknowledgments
We thank Dr Mary Groeneweg for editing the English language version of the manuscript.
Conflict of Interest
The authors declare that there are no conflicts of interest.