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Recurrent painful ophthalmoplegic neuropathy …
- Updated 04.23.2024
- Released 08.22.1995
- Expires For CME 04.23.2027
Recurrent painful ophthalmoplegic neuropathy
Introduction
Overview
Recurrent painful ophthalmoplegic neuropathy, formerly termed “ophthalmoplegic migraine,” is a fascinating and controversial entity. The International Classification of Headache Disorders (ICHD-3) now considers the disorder a cranial neuralgia rather than a type of migraine. Although many cases are typical of a cranial neuralgia, with enhancement of the involved cranial nerve on MRI and improvement using corticosteroids, other cases are more suggestive of a migraine variant. The third nerve is the nerve most frequently involved. Most cases appear in childhood and may persist into adulthood, but onset in adulthood may also occur. The episodes of ophthalmoplegia appear spontaneously and then resolve over days to weeks. As the etiology for recurrent painful ophthalmoplegic neuropathy is likely multifactorial and remains uncertain, the condition may more appropriately be considered a syndrome rather than a distinct diagnosis.
Key points
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• The International Classification of Headache Disorders version 3 classifies recurrent painful ophthalmoplegic neuropathy as a cranial neuralgia. | |
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• MRI of the brain with contrast is recommended for all new cases. | |
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• Although a clinical diagnosis, recurrent painful ophthalmoplegic neuropathy may show enhancement of the involved cranial nerve on post-gadolinium magnetic resonance imaging. | |
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• The third cranial nerve is the most frequently involved nerve in recurrent painful ophthalmoplegic neuropathy. | |
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• Most of the cases start in childhood or early adulthood. | |
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• Episodes of recurrent painful ophthalmoplegic neuropathy appear spontaneously and resolve without treatment. | |
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• Ocular motor nerve schwannomas may produce identical symptoms and resolve spontaneously. | |
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• The etiology for recurrent painful ophthalmoplegic neuropathy is controversial and likely multifactorial, and although a number of treatments have been proposed (eg, steroids, anti-migraine agents), none have proven to be a consistently effective therapy. |
Historical note and terminology
Recurrent ocular motor palsies associated with a headache were previously termed “ophthalmoplegic migraine.” The syndrome most commonly affects the oculomotor (third) nerve, but abducens (sixth) and trochlear (fourth) nerve palsies may occur. The original 1860 report was by Gubler (16; 08), and Charcot first used the term "ophthalmoplegic migraine" in 1890. Gubler's patient subsequently died, and autopsy showed a fibrous mass embedding the third nerve. The patient had no history of migraine but was afflicted with syphilis 10 years earlier. Gowers believed that diplopia was a rare symptom of migraine, and Liveing only briefly alluded to diplopia in his monograph (29; 15). Prior to Charcot's use of the expression "ophthalmoplegic migraine," other synonymous terms included "recurring ocular palsy," "periodic oculomotor paresis," and "recurring third nerve palsy."
Prior to the modern imaging era, authors suggested that ophthalmoplegic migraine represented a congenital anomaly whereby an arteriole at the base of the brain perforated the third nerve or, less commonly, the sixth nerve (19). Alternatively, the involved nerve harbored an occult cavernous hemangioma or other occult vascular malformation. Walsh and O'Doherty cited 200 cases from the literature and postulated that edema of the wall of the carotid within the confines of the cavernous sinus caused pressure on the third nerve, thereby producing an oculomotor nerve palsy involving the pupil (43; 34). In addition to the cavernous sinus, the other potential location for vascular compression is the locus where the third nerve passes between the posterior cerebral and superior cerebellar arteries (32).
Ultimately, demonstrable contrast enhancement of the involved ocular motor nerve on brain MRI in many cases led to replacing the term “ophthalmoplegic migraine” with “recurrent painful ophthalmoplegic neuropathy,” a definable, albeit rare, clinical condition.
Clinical manifestations
Presentation and course
The terms "ophthalmic migraine," or “ocular migraine,” which are erroneously used to describe migraine with visual aura or isolated visual aura without headache, should not be confused with "ophthalmoplegic migraine” or recurrent painful ophthalmoplegic neuropathy. However, adding to the confusion in terminology, the term “ophthalmoplegic migraine” is still pervasive and commonly used colloquially. This article uses “ophthalmoplegic migraine” when referring to citations up to 2002 when Carlow described the MRI findings and questioned the migrainous etiology of the syndrome (06), as the older reports may represent a more heterogeneous group of patients.
The patient with recurrent painful ophthalmoplegic neuropathy typically presents with an otherwise usual but particularly long-lived and severe migraine headache. It is followed by a third or, much more rarely, a sixth (40) or fourth (18) nerve palsy.
Recurrent painful ophthalmoplegic migraine with sixth nerve palsy in a child
A 10-year-old girl had infrequent attacks of recurrent painful ophthalmoplegia affecting the right sixth nerve. She also experienced migraine headaches without ophthalmoparesis, and her mother had migraines without aura. There ...
Rarely, more than one ocular motor nerve is affected (30; 27). Although it may begin at any age, including in adulthood, recurrent painful ophthalmoplegic neuropathy occurs most frequently in infants and children under 12 years of age (28). It occurs as a single event or, more commonly, as recurrent episodes of ophthalmoplegia or ophthalmoparesis.
The headache is typically unilateral, intense, and ipsilateral to the side of the ophthalmoplegia. It has a migrainous phenotype in at least 68% of cases (13; 28). The pain may precede the ophthalmoplegia by several days and is often in the recovery phase before the ophthalmoplegia ensues. Although the headache may alternate sides, bilateral, simultaneous ophthalmoplegia is exceedingly rare (28). In infants, the headache phase may be mistaken for "colic" or "fussiness" (13). Only after the child grows older and is able to describe the symptoms is it apparent that this represents recurrent painful ophthalmoplegic neuropathy. The episodes, which tend to be recurrent and usually improve in the later teenage years, may occur as frequently as weekly or much less frequently. Adult patients may also experience ophthalmoplegic migraines with episodes similar to those in children. The ophthalmoplegia is usually complete but may be partial (superior or inferior branch) third nerve paresis (22). Pupil involvement (mydriasis) is the rule, but on rare occasions, the pupil is not involved (28).
Recurrent ophthalmoplegic migraine with permanent third nerve palsy
This 39-year-old man had ophthalmoplegic migraine episodes at 13 years of age. He had a normal cerebral angiogram. Ophthalmoplegic migraine recurred at 35 years, and multiple attacks left him with a permanent pupil-involving third...
Although the International Classification of Headache Disorders considers ophthalmoplegic migraine a cranial neuralgia since 2004, some controversy remains about the origin and classification of the disorder (14; 24). In the revised International Classification of Headache Disorders, recurrent painful ophthalmoplegic neuropathy (ophthalmoplegic migraine) is part of category 13: painful lesions of the cranial nerves and other facial pain. The criteria are as follows (17):
Recurrent painful ophthalmoplegic neuropathy (13.10). Repeated attacks of paresis of one or more ocular cranial nerves (commonly the third) with ipsilateral headache.
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Diagnostic criteria. | ||
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(A) At least two attacks fulfilling criterion B | ||
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(B) Both of the following: | ||
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1. Unilateral headache | ||
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2. Ipsilateral paresis of one, two, or three ocular motor nerves | ||
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(C) Orbital, parasellar, or posterior fossa lesion has been excluded by appropriate investigations | ||
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(D) Not better accounted for by another ICHD-3 diagnosis | ||
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There are reports of recurrent isolated ptosis as a variant of presumed recurrent painful ophthalmoplegic neuropathy in childhood (41). Recurrent painless oculomotor nerve palsy was proposed as an acephalgic migraine variant in children (10).
Prognosis and complications
Following early attacks, recovery is the rule and usually occurs in 1 to 6 weeks. Later attacks may have the same recovery rate, but the completeness of recovery may be less than satisfactory. Partial ptosis, anisocoria (23), and greater or lesser degrees of permanent disturbance of ocular motility may occur. Rarely, aberrant regeneration occurs.
Clinical vignette
A 42-year-old woman had recurrent painful ophthalmoplegic neuropathy episodes starting at age 8 years. The attacks always affected the left oculomotor nerve and were accompanied by a left-sided migraine headache. The ophthalmoparesis lasted 3 to 4 weeks. The episodes persisted into adulthood, occurring three to four times yearly, always with complete resolution. MR scan during the acute event showed enhancement of the intracisternal portion of the third nerve, which resolved interictally.
Biological basis
Etiology and pathogenesis
Recurrent painful ophthalmoplegic neuropathy is a syndrome that may represent ischemic lesions, inflammation, compressive lesions, or a combination of etiologies. The genetics of recurrent painful ophthalmoplegic neuropathy are unknown, but there is no known familial preponderance. There are no pathologic examinations of this condition because it is not fatal, although one case revealed an atrophic nerve at the level of the posterior cerebral artery at autopsy (32). Cases of aneurysm and tumor coming to autopsy make it clear why this diagnosis has made clinicians wary over the years and why recurrent painful ophthalmoplegic neuropathy is a diagnosis of exclusion.
Liu and colleagues reported five new cases of recurrent painful ophthalmoplegic migraine, some with and some without cranial nerve enhancement on MRI, and they performed a PubMed database literature search from 2000 to 2020 (28). They analyzed 52 articles containing 165 patients. The female-to-male ratio was 1.4:1, with an average age at onset of 22.1 years (range 3 months to 74 years). However, when an accurate age of onset was reported, 50 of 76 (65.8%) patients had their initial attack before the age of 18. The most common headache phenotype was migraine in 87.9%, and 6.1% of patients did not have a history of migraine. The headache location varied and was specified in only 60 cases; almost half of them had periorbital pain. The pain was always ipsilateral to the ophthalmoplegia (n=77). Only 31.5% of patients had a family history of migraine.
The frequency of attacks ranged from once in several years to several times per month. The interval between the onset of headache and the onset of ophthalmoplegia was generally within 1 week (n=62), ranging from simultaneously (n=5) to 15 days (n=1). Two patients developed the ocular motor paresis prior to the headache. The oculomotor nerve was the most commonly affected. Two patients had bilateral involvement with no side predominance identified overall. Of the 78 cases with a third nerve palsy including pupil information, 55.1% of them had mydriasis.
Table 1. Ocular Motor Nerves Involved in Recurrent Painful Ophthalmologic Neuropathy
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All cases (N=165) | ||
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Nerve(s) involved |
Number |
Percent |
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Oculomotor (III) |
89 |
53.9 |
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Trochlear (IV) |
6 |
3.6 |
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Abducens (VI) |
61 |
37.0 |
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Two nerves combined |
7 |
4.2 |
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Cases with onset before the age of 18 (N=50) | ||
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Nerve(s) involved |
Number |
Percent |
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Oculomotor (III) |
47 |
94 |
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Trochlear (IV) |
1 |
2 |
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Abducens (VI) |
0 |
0 |
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Two nerves combined |
2 |
4 |
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Cases with onset after the age of 18 (N=26) | ||
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Nerve(s) involved |
Number |
Percent |
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Oculomotor (III) |
14 |
53.8 |
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Trochlear (IV) |
0 |
0 |
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Abducens (VI) |
10 |
38.5 |
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Two nerves combined |
2 |
7.7 |
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Not specified |
2 |
n/a |
|
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The controversy regarding the etiology of recurrent painful ophthalmoplegic neuropathy as a demyelinating cranial neuropathy or a form of migraine largely centers around the presence or absence of ocular motor nerve enhancement on MRI. Liu and colleagues found that 40 of 145 patients (27.6%) who had a contrast-enhanced MRI showed thickening and/or enhancement of the cranial nerve. Those with childhood onset were significantly different from patients with adult onset in this regard. Abnormalities of at least one involved cranial nerve were present in 31 of 49 (63.3%) childhood-onset patients compared to 9 of 26 (34.6%) adult-onset patients (p=0.28). As 105 patients had no abnormality on a contrast-enhanced MRI, it is plausible that migraine was the etiology in most patients.
Shin and colleagues performed SPECT during an attack of ophthalmoplegic migraine. A significantly decreased regional cerebral blood flow in the ipsilateral thalamus reverted to normal. The authors postulated that reversible ischemia in the perforators of the posterior cerebral arteries may be a contributing feature (38).
Vieira and colleagues reported a 7-year-old boy with an infundibular dilation of a perforating branch of the posterior cerebral artery with presumed compression on the symptomatic third nerve, and these authors speculated that this might be another mechanism for trigeminovascular system activation (35). Ischemic reversible breakdown of the blood-nerve barrier was also postulated (04).
Lance and Zagami proposed recurrent demyelinating neuropathy as a mechanism (25). Carlow reported six cases with thickening and enhancement of the involved third nerve. He proposed that the pathophysiology might be related to a trigeminovascular migraine epiphenomenon dependent on the anatomy of the third nerve, a porous blood-brain barrier, and demyelination (06). Although the possibility of an underlying structural lesion (eg, cavernous malformation) within the oculomotor nerve has been raised, there is little clinical or pathological evidence to support this theory (26). Akimoto and colleagues reported a case of biopsy-confirmed neuromuscular hamartoma at the root exit zone and proposed that trigeminovascular stimulation could lead to dilation of the blood vessels that supply the oculomotor nerve. The vascular dilation could induce muscle contraction of the neuromuscular hamartoma, leading to possible strangulation of the oculomotor nerve and ophthalmoplegia (03).
Many patients with recurrent painful ophthalmoplegic neuropathy are empirically treated with corticosteroids, particularly if the affected cranial nerve enhances on MRI. Corticosteroid treatment complicates the diagnosis during the initial presentation, as secondary causes such as tumors, lymphoma, and demyelination may also improve with corticosteroid treatment. Therefore, a proposed classification scheme endorsed a primary migrainous etiology as well as a secondary cause, with the distinction based on the MRI scan and natural history without corticosteroid treatment in at least one event (12).
Supporting a migraine etiology, there is a strong correlation between migrainous attacks and ophthalmoplegia. Over 90% of patients have typical migraine headaches prior to the onset of ophthalmoplegia, supporting a migrainous process in patients without an ocular motor nerve enhancement on MRI. Moreover, the trochlear and abducens nerves lack pain-sensitive fibers, and enhancement of the involved nerve in pediatric patients may be related to relative immaturity of the blood-nerve-barrier (24). Lal and Caplan postulated that activation of proinflammatory neuropeptides during a migraine attack may cause breaching of the blood-brain barrier and subsequent edema or ischemia of the nerve with or without gadolinium enhancement (24). Others proposed a classification schema that distinguishes childhood from adult onset, with or without thickening/enhancement of the affective cranial nerve (07).
Epidemiology
The estimated incidence in childhood is 0.7 per million (40). A study from India identified 18 new adult cases of recurrent painful ophthalmoplegic neuropathy among approximately 4000 headache patients over a 5-year period; most patients had sixth nerve palsies, which is not typical of the general reported experience favoring third nerve palsies (07). Only one case was identified in a study of 111 migraine patients in a pediatric practice (36). No matter the venue, it is a rare condition.
Prevention
Previous recommendations suggested treating ophthalmoplegic migraine with preventive medications as in other types of migraine, with a preference for calcium channel blockers. However, given that recurrent painful ophthalmoplegic neuropathy is no longer felt to be of migrainous origin, standard migraine prevention is likely ineffective.
Differential diagnosis
The differential diagnosis includes conditions that can produce unilateral head pain and ipsilateral ophthalmoplegia (40). Intracranial aneurysm must be excluded, particularly with third nerve involvement. Microvascular ocular motor cranial nerve palsies may be associated with ipsilateral pain and are a likely cause of misdiagnosed cases of adults with recurrent painful ophthalmoplegic neuropathy in the literature. The Tolosa-Hunt syndrome is a painful ophthalmoplegia syndrome arising from the cavernous sinus with pain that persists long after the ocular motility defect appears. It is associated with multiple cranial nerve involvement, proptosis, and conjunctival injection (05). The ICHD-3 criteria allow for the presence of simultaneous, ipsilateral third, fourth, and sixth nerve palsies with recurrent painful ophthalmoplegic neuropathy; however, the diagnosis is made with extreme caution in such cases. Recurrent painful ophthalmoplegic neuropathy generally affects only one ocular motor nerve. Reliance on MRI to distinguish Tolosa-Hunt syndrome from recurrent painful ophthalmoplegic neuropathy is unreliable as the MRI is normal in up to half of the cases of Tolosa-Hunt syndrome (01). Other diagnostic considerations include sphenoid sinus mucoceles, cavernous sinus, sellar and parasellar tumors (eg, pituitary apoplexy), and sinus infections (eg, fungal) (33).
At least one patient with ophthalmoplegic migraine had an internal carotid artery dissection with a tapered occlusion but no hemiparesis or other evidence of ischemia (09).
Diabetic neuropathies and neuropathies associated with collagen vascular disease, granulomatosis with polyangiitis (Wegener), and idiopathic orbital inflammation (inflammatory orbital pseudotumor) may produce the same constellation of unilateral head pain with ocular motor nerve and orbital symptoms (33). The major differential clue is that patients with RPON have a headache, which is usually excruciating, a day or more before the onset of ophthalmoplegia, which usually appears as the pain is abating. Painless attacks of oculomotor palsy are very rare and may precede the development of migraine headaches in children (10).
A previous history of similar spells and relative youth at onset of symptoms should point to the correct diagnosis, but recurrent painful ophthalmoplegic neuropathy remains a diagnosis of exclusion. The relevance of a personal or family history of migraine is uncertain given the controversial pathogenesis of the disorder and the high population prevalence of migraine.
Schwannoma of the third cranial nerve can produce a similar MR appearance and mimic the clinical presentation of recurrent painful ophthalmoplegic neuropathy (02). Shin and colleagues reported 10 cases of patients with ocular motor nerve schwannomas, four of which involved the third nerve, four affected the fourth nerve, one involved the sixth nerve, and one affected the third and sixth nerves in Meckel cave (39). Of the three patients with headaches, all had third nerve palsies, and two had a history of migraine. An oculomotor nerve mass with radiographic features of schwannoma was discovered in a patient with a 20-year history of recurrent painful ophthalmoplegic neuropathy attacks with incomplete resolution, corticosteroid side effects, and previously normal neuroimaging (02). Linear accelerator-based hyperfractionated stereotactic photon radiotherapy produced a reduction in symptoms, improvement in his exophoria, and disappearance of ptosis.
Some researchers proposed that a form of recurrent painful ophthalmoplegic neuropathy exists that consists simply of isolated pupillary dilation associated with headache (31); however, benign episodic pupillary mydriasis is a separate entity from recurrent painful ophthalmoplegic neuropathy. In these cases, the pupil is large and reacts little, if at all, to light (21). The "tadpole pupil" is a rare condition of segmental spasm causing a tadpole-shaped pupil, resulting in unilateral pupillary dilation lasting minutes to hours (42). It occurs more frequently in women. Unlike episodic mydriasis, the tadpole pupil is teardrop or oval-shaped.
One should carefully exclude episodes of unilateral angle closure glaucoma with pupillary block when considering the diagnosis of severe, unilateral headache associated with pupillary dilation and a red eye, particularly in a patient with migraine who is taking topiramate for prophylaxis (11).
Diagnostic workup
A sedated MRI with contrast and MRA should suffice for an infant or young child. When a patient over 12 years of age has a third nerve palsy, it is imperative to rule out internal carotid-posterior communicating aneurysms with MR angiography, CT angiography, or digital subtraction angiography; the risk of the procedure is low and the benefit, if an aneurysm is found, is great. During an attack, MRA and MR scans focusing on the anatomical locations of cranial nerves III, IV, or VI, may help to delineate the condition. Some authors suggest that cerebral angiography is unnecessary in the presence of gadolinium enhancement of the third nerve. The gadolinium enhancement is usually in the interpeduncular space and cisternal segment on MR scans (13; 40). The enhancement and thickening of the oculomotor nerve in recurrent painful ophthalmoplegic neuropathy is generally transient and almost completely resolved by 7 to 9 weeks (28). However, some patients have no pathologic enhancement on the MRI.
Detailed MR imaging of the cavernous sinuses with gadolinium is needed, especially when Tolosa-Hunt syndrome is suspected. The parasellar regions, cavernous sinuses, pituitary fossa, suprasellar space, interpeduncular spaces, clivus (in the case of the sixth nerve), and the tentorial edge (in the case of the fourth nerve) should be scrutinized. Lumbar puncture and clinical evaluation for infiltrative (eg, lymphoma and leukemia) and infectious etiologies may be necessary in some cases.
Management
As recurrent painful ophthalmoplegic neuropathy is so rare, and the cases reported in the literature so heterogeneous, there is little evidence to guide therapy. Symptomatic treatment with a course of corticosteroids may shorten the duration of the attack and severity of the pain (10; 06; 13; 40; 28). Some cases resolve spontaneously, although such patients typically need pain control. Ishikawa and colleagues reported a remarkable case in which topical administration of 0.25% timolol maleate twice daily to both eyes reduced the frequency and symptoms of migraine (20).
In their literature review, Liu and colleagues found that 78 of 165 patients were treated with corticosteroids alone (36/78) or in combination with antimigraine treatment (42/78), and this was effective in 75 of 78 patients (96.2%). Three patients reported worsening with corticosteroids (28). These results contain bias, however, as 34 patients (69.5%) declined corticosteroid treatment and were consequently treated with antimigraine treatment only, including beta blockers and calcium channel blockers. Six patients responded to indomethacin (37), and the addition of corticosteroids to antimigraine treatment seemed to hasten recovery.
Outcomes
An analysis of 15 of 165 patients with detailed data regarding the onset and resolution of the headache and ophthalmoplegia reported resolution of the headache within 4 days in nine patients and by 2 weeks in the other five patients (28). The ophthalmoplegia recovered within one day in a single patient and within a week in two patients. Ocular motor paresis lasted a week or more in the other 12 patients. The longest duration was nearly 12 weeks. Up to 30% of patients experienced permanent neurologic sequela after repeated attacks (40; 28).
Media
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Contributors
All contributors' financial relationships have been reviewed and mitigated to ensure that this and every other article is free from commercial bias.
Author
-
Deborah I Friedman MD MPH
Dr. Friedman received honorariums from Abbvie, Impel, Invex Therapeutics, Lundbeck, Pfizer, Revance, Satsuma, Supernus, and Theranica as an advisory board member, medical advisor, or speaker; she received grant support from Eli Lilly as an advisory board member and speaker.
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Editor
-
Stephen D Silberstein MD
Dr. Silberstein, Director of the Jefferson Headache Center at Thomas Jefferson University has no relevant financial relationships to disclose.
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Former Authors
- James Corbett MD (original author), Andrew G Lee MD, Paul W Brazis MD, and Priyanka Chaudhry MD
Patient Profile
- Age range of presentation
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- 1 month to 44 years
- Sex preponderance
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- male>female, >1:1
- Heredity
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- none
- Population groups selectively affected
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- none selectively affected
- Occupation groups selectively affected
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- none selectively affected
ICD & OMIM codes
- ICD-9
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- Ophthalmoplegic migraine: 346.8
- ICD-10
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- Ophthalmoplegic migraine: G43.8
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