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Abstract

To investigate the relevance of lacking or diminished visual input on the expression of migraine, we evaluated its prevalence and clinical features in a population of visually impaired subjects. Between September 1999 and April 2000, 203 visually impaired subjects with a headache inventory were surveyed. Those with headache were assessed according to IHS criteria for the presence of migraine. Migraineurs had their symptoms further detailed through an interview and a headache diary. Of the 104 subjects reporting headaches during the last 6 months, 29 had migraine (14.2%). The prevalence of migraine was not influenced by whether the visual impairment was complete or partial. Mean frequency of migraine attacks was 2.7/month. Most subjects (96%) reported severe and/or moderate attacks. Nausea, vomiting, aggravation by activity and phonophobia were reported by 62%, 37.9%, 86.2% and 96.6% of the subjects, respectively. Visual impairment does not seem to influence prevalence of migraine or its clinical features.

Keywords

Blindness migraine visual impairment

Introduction

The relationship between migraine and the visual system is not limited to the occurrence of visual aura (1) and photophobia (2), but to several ictal and interictal functional peculiarities of the pathways related to visual input and processing (1–7). Drummond (2) has shown that migraineurs present higher glare ratings to light stimulation between migraine attacks, compared with controls. When submitted to flicker stimulation, most migraine subjects present a driving response of their alpha rhythm (3). Potentiation instead of habituation of interictal visual evoked responses to checker-board pattern stimulation is seen in migraineurs compared with controls (4). Wray et al. (5) have shown migraineurs to present a greater sensitivity for low-level visual processing between attacks, a finding suggestive of functional impairment of inhibitory interneurones. Evidence for such impairment has been more recently presented by Mulleners et al. (6), by showing that inhibition of letter recognition at 100 msec was less disturbed by transcranial magnetic stimulation in migraineurs than in controls. Compared with healthy volunteers, migraineurs present lower thresholds for visual discomfort when exposed to progressive light stimuli (8–10). The wave of spreading hypoperfusion that has been shown to occur during attacks of migraine with or without aura usually starts in the occipital lobes before spreading forward (11–13).

Recently, we have shown that intense light stimulation could lower trigeminal and cervical pain perception thresholds (10), a finding that suggested that visual input, by lowering pain thresholds, could facilitate migraine attacks. We have conducted this study in order to determine if the lack of light input or a status of diminished light perception in visually impaired individuals could influence the prevalence and clinical features of migraine.

Population and methods

Between the months of September 1999 and April 2000, 208 subjects from eight centres for visually impaired subjects in Curitiba, Brazil, were randomly recruited. They were personally interviewed, answering structured questions regarding the occurrence of headache in their lifetime. Inclusion criteria were both genders, aged between 16 and 60 years, and presence of total blindness or of a severe visual impairment. Exclusion criteria were cognitive dysfunction, inability to identify more than one type of headache when present, lack of will to participate, and progressive neurological disease. Five patients were excluded, one due to lack of will to participate, two due to the presence of associated psychiatric disorders, and two because of cognitive impairment. Those with headaches were further assessed according to IHS criteria (14) for the occurrence of migraine in their lifetime, in the last year, in the last 6 months, and in the last month. Migraineurs were submitted to an additional inventory to obtain further details of the clinical features of their migraine attacks. All data were collected on a person-to-person basis. They were also submitted to another ophthalmologic evaluation, and were asked to fill out a headache diary with a tactile analogical scale for pain (TAS) (15), specially designed for the study. Regarding their visual impairment, those without any perception of visual stimuli in both eyes were classified as totally blind (ICD-10 category 5), and those with subnormal vision or ‘legally blind’ (ICD-10 categories 1–4), in whom even after the best optical correction visual acuity in the best eye remained 20/200 (category 1) or lower (categories 2–4, 16). anova, comparison of the proportions (CP test), Mann–Whitney and Student's t-test were used to compare data of those totally blind with the findings of those with subnormal vision. Demographics of the population and aetiology of visual impairment are shown in Table 1.

Table 1

Demographics and clinical features of the study population

	Migraineurs		Non migraineurs		Total
	n	%	n	%	n	%
	29	14.3	174	85.7	203	100
Gender
Males	7	24.1	118	67.8	125	61.6
Females	22	75.9	56	32.2	78	38.4
Age (years± SD)	31	± 10.7	36.0	± 16.5	35.3	± 15.9
Aetiology
Congenital	13	44.8	95	54.5	108	53.2
Acquired	13	44.8	62	35.6	75	36.9
Congenital+acquired	3	10.4	14	8.0	17	8.4
Unknown	–	–	3	1.7	3	1.5
Specific aetiology
Cataract	8	27.6	34	19.5	42	20.7
Glaucoma	2	6.9	32	18.4	34	16.8
Trauma	1	3.4	13	7.5	14	6.9
Retinal detachment	1	3.4	12	6.9	13	6.4
Tumour	3	10.4	8	4.6	11	5.4
Measles	2	6.9	8	4.6	10	4.9
Pigmentary retinosis	1	3.4	6	3.4	7	3.4
Others	7	24.2	32	18.4	39	19.2
Unknown	4	13.8	29	16.6	33	16.2

Results

Of the 203 patients interviewed, migraine was diagnosed for any period of life in 34 (16.7%). One patient had not had any headache episode in the last 6 years, one patient had his migraine transformed to a chronic daily headache and in a third patient migraine subsided and a tension-type headache ensued. Thirty-one patients complained about migraine episodes in the last year (15.3%), but two of them had not presented any migraine episode in the last 6 months. Four patients reported another headache associated with migraine: one reported idiopathic stabbing headache, another, headache associated with arterial hypertension, and two others reported tension-type headaches. All of them knew how to distinguish their other headaches from migraine.

Our results showed a prevalence ratio for migraine of 14.28% for the 6 months preceding the study. Of the 29 visually impaired subjects presenting with migraine in the 6 months preceding the study, seven were male and 22 female. Mean age was 30.6 ± 10.2 years, and there was no difference of age between those totally blind (32.2 ± 7.5 years) and those with subnormal vision (29 ± 11.7 years) (P = 0.612, Mann–Whitney). There was no difference in migraine prevalence in the totally blind compared with those with subnormal vision (P = 0.735, CP test). Twenty-five subjects (12.3%) had at least a single migraine attack in the month preceding the appointment. Additional details of prevalence data are shown in Table 2.

Table 2

Prevalence of migraine in the subjects studied. Visually impaired subjects (n = 203)

Prevalence	All the migraineurs		Totally blind (ICD-10 category 5)		Subnormal vision (ICD-10 categories 3–4)
Prevalence	n	%	n	%	n	%
Last month	25	12.3	8	10.3	17	13.6
Last 6 months	29	14.3	11	14.1	18	14.4
Males∗	7	24.1	3	27.3	4	22.2
Females∗	22	75.9	8	72.7	14	77.8
Last year	31	15.3	12	15.4	19	15.2
Lifetime	34	16.7	14	18.0	20	16.0

n, number of subjects; ICD=International Classification of the Diseases;

^∗data based on the last 6 months' prevalence.

Characteristics of migraine in those patients presenting with migraine attacks in the 6 months preceding the study were further detailed. They presented a mean of 2.7 attacks in the month preceding the study, with a mean duration of 27.5 h. Unilateral pain during the attacks was reported by 41.37% of the subjects. Phonophobia was reported by 96.55% of the migraineurs. Photophobia was present in 61.1% of the 18 patients with subnormal vision. Nausea and vomiting were present in 62% and 37.9% of the patients, respectively. Most of the patients (86.2%) reported aggravation of the symptoms by activity. Migraine episodes were reported as severe by 58.6% of the patients. Although patients with subnormal vision reported severe attacks more frequently than those totally blind, this difference was not statistically significant (P = 0.969, CP test). Four female patients reported migraine with aura. Aura was reported to be auditory by one and visual by three. The auditory aura patient was totally blind and described her auditory aura as bilateral tinnitus. Two of the visual aura patients had subnormal vision, and visual aura was described by both as scintillating scotomata lasting 2–4 min, usually preceding the headaches.

The other visual aura patient had had migraine headaches since adolescence, sometimes preceded by bilateral scintillating scotomata lasting 1 min. She started suffering a progressive visual loss at the age of 30 and her visual aura disappeared. An occipital meningeoma was diagnosed and resected and in the 4 years of follow-up she has remained a migraineur, although her migraine visual aura has remitted. The clinical features of the migraine attacks in the visually impaired patients that reported migraine episodes in the last 6 months are summed up in Tables 3 and 4.

Table 3

Characteristics of the migraine headaches∗

	Totally blind (n = 11)†		Subnormal vision (n = 18)‡		P ∗∗	Total (n = 29)
	n	%	n	%	P ∗∗	n	%
Duration in hours
4–12	3	27.3	5	27.8	0.694	8	27.6
13–24	4	36.4	8	44.4	0.971	12	41.4
25–72	2	18.2	4	22.2	0.830	6	20.7
Not available	2	18.2	1	5.6	0.651	3	10.3
Characteristics of pain
Throbbing	10	90.9	13	72.2	0.463	23	79.3
Compressive	–		4	22.2	0.259	4	13.8
Mixed	1	9.1	1	5.6	0.694	2	6.9
Intensity of pain
Mild	–		1	5.6	0.806	1	3.5
Moderate	5	45.5	6	33.3	0.793	11	37.9
Severe	6	54.5	11	61.1	0.969	17	58.6
Laterality of pain
Bilateral	4	36.4	7	38.9	0.795	11	37.9
Unilateral	4	36.4	8	44.4	0.971	12	41.4
Shifting sides	3	27.2	3	16.7	0.838	6	20.7

n, number of subjects;

^∗data based on the migraine headaches occurring in the last 6 months;

^†ICD-10 category 5;

^‡ICD-10 categories 1–4;

^∗∗CP test.

Table 4

Characteristics of the associated symptoms∗

Totally blind (n = 11)†		Subnormal vision (n = 18)‡			Total (n = 29)
	n	%	n	%	P §	n	%
Aggravation by activity
Present	10	90.9	15	83.3	0.983	25	86.2
Not present	–	–	3	6.7	–	3	10.4
Unknown	1	9.1	–	–	–	1	3.4
Anorexia	8	72.7	11	61.1	0.814	19	65.5
Nausea	7	63.6	11	61.1	0.795	18	62.1
Vomiting	4	36.4	7	38.9	0.795	11	37.9
Photophobia
Present	–	–	11	61.1	0.004	11	37.9
Not present	–	–	6	33.3	–	6	20.7
Unknown	–	–	1	5.6	–	1	3.5
Not applicable∗∗	11	100	–	–	–	11	37.9
Phonophobia	11	100	17	94.4	0.806	28	96.6
Aura	2	27.2	2	11.1	0.543	4	13.8

n, number of subjects;

^∗data based on the migraine headaches occurring in the last 6 months;

^†ICD-10 category 5;

^‡ICD-10 categories 1–4;

^§CP test;

^∗∗blind subjects.

The findings obtained through the application of the TAS will be presented elsewhere.

Discussion

Prolonged exposure to the glare of intense light, particularly to sunlight, has been reported by 30% to 45% of migraineurs to trigger migraine attacks (17, 18). The patient with migraine without aura and with a spreading oligemia described by Woods et al. presented an attack when submitted to complex visual stimuli (12). More recently, Cao et al. have reported attacks of migraine with aura triggered by specific visual stimuli (19). After Moskowitz hypothesized on the role of the trigeminal vascular system in migraine pain (20), Lance postulated the neurovascular hypothesis, emphasizing the role of endogenous or environmental stimuli over the hypothalamus and its efferent pathways projecting to brainstem nuclei, such as the locus coeruleus or the raphe nuclei, on the triggering of migraine attacks (21). Recently, we have shown light stimulation to induce not only discomfort in migraineurs at lower levels than in controls, but also to lower their trigeminal and cervical pain perception thresholds (10), a finding that suggested that visual input, by lowering pain thresholds, could facilitate migraine attacks.

Conversely, attacks beginning in the absence of light, i.e. during sleep, are known to happen in migraineurs (22). Peatfield and Rose have described the case of a woman whose eyes were enucleated in her early childhood, who started to present migraine with aura soon afterwards (23). Her migraine with aura attacks persisted through her childhood, adolescence and adulthood in spite of the lack of visual input.

Disorders of the eyes leading to blindness, especially acute glaucoma, are known to be associated with pain in the head or in the eye. However, the clinical features of headaches related to eye pathology usually differ from those of migraine (14), although they may rarely mimic migrainous features (24). Pradalier et al. (25) have reported a high prevalence of migraine in a population of patients with glaucoma, a finding that has to be carefully interpreted, as the questionnaire used to diagnose migraine was applied by ophthalmologists not familiar with that condition.

Interestingly enough, the clinical features of migraine attacks described by our patients were very similar to those reported by visually normal individuals (26, 27), but phonophobia was reported at a higher proportion by the visually impaired. Surprisingly, photophobia was reported by a still higher proportion of the individuals with partial visual impairment, in spite of the fact that most of these patients could barely perceive light stimuli. The fact that most patients presented severe visual impairment might explain the lack of significance of the finding of more severe attacks by subjects with partial rather than complete visual impairment, as a larger population would be needed to reach a definite conclusion. There were no differences between the other features of the migraine attacks on totally blind individuals and on those with subnormal vision.

Our prevalence numbers were lower than those found by Bigal et al. (28) and by Sanvito et al. (29) in Ribeira~o Preto and Sa~o Paulo, mid-eastern Brazil, but these authors have carried out their studies on highly selected populations, as they searched for the prevalence of migraine among the personnel of a university hospital and among medical students, respectively. The study of Barea et al. in Porto Alegre, southern Brazil, reported lower numbers, but it was carried out on a population of a rather lower age bracket (30). The fact that the population studied is highly Caucasian might explain why the migraine prevalence numbers found were very similar to those described in some population-based studies carried out in the northern hemisphere (31, 32). Curitiba is the capital of the state of Paraná, in south–eastern Brazil, located 900 m (3000 feet) above sea level, near the Atlantic margin of the Brazilian Highlands and the headwaters of the Iguaçu river. Since 1654 it has been colonized by Caucasians of Portuguese ancestry. From 1854 to 1914 it received many Italian, German and Polish immigrants, a smaller wave of Syrians and Japanese coming later (33). Caucasians predominated in the 1991 census as Whites made up 81.7% of its population (34), followed by 15.7% of Mulattos, 1.7% of Blacks, and 0.9% of Amerindians and Orientals (34). Further HLA analysis of the different sub-populations confirmed Portuguese, Italian, German and Polish Caucasian haplotypes in 94% of the White population. The other sub-populations revealed a more pronounced interethnic admixture, with Caucasian haplotypes found in 57% of the Mulattos and 25% of the Black population (35).

According to our results, complete or partial visual impairment seems not to affect the prevalence of migraine, as they suggest that lacking or diminished light input does not affect the expression of migraine on predisposed individuals. Our subjects derived from an estimated population of approximately 11 200 visually impaired individuals (36), being thus representative (1.8%). However, our sample of migraine patients was small and a type two error in the statistical analysis cannot be completely excluded.

The finding that the prevalence of migraine is unaffected by diminished or lacking light input suggests that the environmental visual stimuli play a secondary role in the expression of migraine. However, as suggested by the report of phonophobia by most of the patients and of photophobia by the subjects with subnormal vision, the role played by each sensorial channel on migraine expression may depend on the level of activity of that specific sensorial channel in a given individual.

Although our findings suggest that normal visual processing is not a sine qua non condition for the expression of migraine, the role of the visual system on migraine pathophysiology remains a challenge to be clarified.

Footnotes

Acknowledgements

The authors express their gratitude to Ms Miria de Souza Fagundes Leonardi, for introducing us to associations of visually impaired subjects, to Ms Angela da Matta Silveira Martins, for statistical support, and to Mr Nelson Torres, for the review of language. Dr Salmo Raskin has helped us regarding the genetic aspects of the population of Curitiba. This work was partially supported by a CNPq PIBIC grant.

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Prevalence and Clinical Features of Migraine in A Population of Visually Impaired Subjects in Curitiba,Brazil

Abstract

Keywords

Introduction

Population and methods

Results

Discussion

Footnotes

Acknowledgements

References