Seminars in Ophthalmology

ISSN: 0882-0538 (Print) 1744-5205 (Online) Journal homepage: http://www.tandfonline.com/loi/isio20

Skew Deviation: Case Report and Review of the
Literature
Katarina Ivana Tudor, Damir Petravić, Anđela Jukić & Zlatko Juratovac
To cite this article: Katarina Ivana Tudor, Damir Petravić, Anđela Jukić & Zlatko Juratovac
(2016): Skew Deviation: Case Report and Review of the Literature, Seminars in Ophthalmology,
DOI: 10.3109/08820538.2016.1170164
To link to this article: http://dx.doi.org/10.3109/08820538.2016.1170164

Published online: 29 Jul 2016.

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Date: 01 August 2016, At: 07:32

Seminars in Ophthalmology, Early Online, 1–4, 2016
© Taylor & Francis
ISSN: 0882-0538 print / 1744-5205 online
DOI: 10.3109/08820538.2016.1170164

ORIGINAL ARTICLE

Skew Deviation: Case Report and Review of the
Literature
Katarina Ivana Tudor1, Damir Petravić1, Anđela Jukić2, and Zlatko Juratovac3
Department of Neurology, University Hospital Center Zagreb, Zagreb, Croatia, 2Department of
Ophthalmology, University Hospital Dubrava, Zagreb, Croatia, and 3Department of Ophthalmology,
University Hospital Center Zagreb, Zagreb, Croatia

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1

ABSTRACT
Objective: To present a patient with a sudden onset ocular tilt reaction (OTR) and review recent knowledge and
evolving insights of the underlying pathophysiological mechanisms of skew deviation and OTR. Methods: A
middle-aged hypertensive man who had previously suffered stroke with good recovery presented with suddenonset double vision, slurred speech, ataxia, and a head tilt. Romberg test was positive. The patient denied having
disturbances of visual acuity, eye pain, or recent trauma. The right eyeball was pushed upward. The patient
complained of double vision in any gaze direction. Movements of the extraocular muscles (EOMs) in the
horizontal plane were normal, whereas vertical version and convergence were not possible. We administered a
Hess-Lancaster test, cover test, fundoscopic examination, Parks-Bielschowsky three-step test, upright-supine test,
brain magnetic resonance imaging (MRI), transcranial doppler (TCD) ultrasonography, electrocardiogram (ECG),
Holter monitor (24 h), and echocardiography. Results: The Hess-Lancaster test showed superior rectus muscle
and inferior obliquus muscle palsy to the left and rectus inferior muscle and superior obliquus muscle palsy to
the right. The right eyeball fell behind when looking downward and the left eyeball when looking upward.
Cover alternating test was positive from vertical, R/L. Examination of the ocular fundus showed incyclotorsion
of elevated right eye and excyclotorsion of depressed eye. The Parks-Bielschowsky three-step test was negative.
A brain MRI with gadolinium revealed a small zone of diffusion restriction in the medial portion of the right
cerebral peduncle and right thalamus. There was a gradual improvement in the patient’s neurological status
following treatment. Conclusion: Skew deviation, a not uncommon clinical condition, should be promptly
recognized when binocular vertical diplopia cannot be interpreted by trochlearis and oculomotor nerve lesion,
myasthenia gravis, or orbital pathology. Maddox rod, cover test, Parks-Bielschowsky three-step, and other tests
should help to establish the diagnosis. The prognosis depends on etiology, but it is commonly favorable; the
majority of patients recover spontaneously after less than a year. More invasive management options should be
discussed thereafter.
Keywords: Neuro-ophthalmology, ocular tilt reaction, skew deviation, strabismus, stroke, vertical double vision

and neurotological insights have proved the opposite.7
Pathological conditions that affect the brain stem,
cerebellum, or peripheral vestibular system may initially present (among other neurological signs) with
skew deviation.1,2,7 Magendie and, later,Hertwig
were the first to describe this condition in animals in
1824. Stewart and Holmes reported vertical strabismus
in a patient with a cerebellar tumor and, later on,
following gunshot wounds to the head. Keane was
the first to propose an imbalance of the otolith-ocular
reflex as a possible cause of skew deviation, and

INTRODUCTION
For more than a century, Hertwig-Magendie sign or
skew deviation have been used to denote acquired
vertical strabismus caused by supranuclear posterior
fossa pathology.1–5 Some suggest that this was the
transitory eye condition that Michelangelo suffered
while painting the Sistene Chapel in Rome in 1510.6
Although for many years wrongly assumed to be of
nonlocalizing value, evolving neuroopthalmological

Received 28 November 2015; accepted 16 March 2016; published online 30 July 2016
Correspondence: Katarina Ivana Tudor, MD, Department of Neurology, University Hospital Center Zagreb, Kispaticeva 12, 10 000 Zagreb,
Croatia. E-mail: tudorkatarinaivana@gmail.com

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K. I. Tudor et al.

asymmetric disruption of otolithic projections to oculomotor and trochlear nuclei as the underlying pathological mechanism, and stressed the possible role of
polysynaptic pathways via the cerebellum. Brandt and
Dietrich described ipsiversive skew deviation as a
localizing sign of a pontomedullary lesion, while contraversive skew deviation was found to implicate more
rostral, pontomesencephalic lesions.2,7–9
In humans, achieving normal oculomotor activity is
dependent upon a complex interplay between complex
supranuclear circuitry, brainstem nuclei, cranial nerves
III, IV, and VI, their respective neuromuscular junctions, target muscles, and otolith organs that consist of
the utricle and saccule.10 The utriculo-ocular reflex is
responsible for detection of horizontal head translation
and static head tilt. It transmits information to the
midbrain, vertically acting ocular motoneurons, as
well as to the interstitial nucleus of Cajal (INC). An
imbalance of underlying pathways can cause asymmetric reduction of the translational vestibulo-ocular
and ocular counter-roll responses and result in skew
deviation. 11,12

TABLE 1. Conditions presented with skew deviation.
Condition

Diagnosis

Neurogenic

Stroke
Brain hemorrhage
Traumatic brain injury
Unruptured intracranial aneurysms
Demyelinating lesion
Brain tumor
Abscess
Raised intracranial pressure
Hashimoto encephalopathy
Infection (Ramsey-Hunt syndrome, central
nervous system cryptococcosis)
Paraneoplastic encephalomyelitis
Creutzfeldt-Jakob disease
Epilepsy
Syringobulbia
Arnold-Chiari malformation
Spinocerebellar ataxia types 3 and 6
Neurosurgical procedures after resection of
the cerebellopontine angle tumor, deep
brain stimulation (DBS)
Acute unilateral vestibular organ lesion
Vestibular neuritis
Post-surgery complication after
labirinthectomy, vestibular nerve surgery
Hepatic coma
Transient complication of cardiac
catheterization (ischemic strokes not
detected on neuroimaging)
• Carbamazepine

Otogenic

Internal medicine

Drug-induced

● Consequent to oral or intravenous admin-

istration of diphenylhydantoin and
amitriptyline
● Intratympanic gentamicin therapy for the

treatment of episodic vertigo

Both peripheral and central conditions may present
with skew deviation1,2,5,7,13–30 (Table 1).
The most common cause of skew deviation is brainstem stroke. Additional forms, such as paroxysmal
skew deviation (noise induced due to perilymph fistula—Tullio phenomenon), alternating skew deviation,
and transient neonatal skew have been recognized.7
Classical skew deviation usually occurs as a part of
ocular tilt reaction (OTR), a clinical syndrome characterized by a complex interplay of perceptual (tilt in
subjective vertical), ocular motor (tonic or paroxysmal
ocular torsion; and skew deviation), and postural
(head tilt) manifestations.7
OTR and skew deviation are usually ipsiversive
with peripheral and pontomedullary lesions, and
contraversive with pontomesencephalic lesions; i.e.,
if the brain lesion occurs prior to crossing the pathway, the lower eye will be on the same side as the
lesion, and if the lesion is higher in the brain (after
pathways crossing), the higher eye will represent the
side of the lesion. In thalamus lesions, the tilts of the
subjective visual vertical may be contraversive or
ipsiversive.7,31 By convention, the term hypertropia
is used (regardless of the lesion site) to denote the
higher eye, regardless of which is at fault. Three
different types of skew deviation are described
when they occur as a part of OTR: upward deviation
of both eyes (lesion site in utricle; e.g., Tullio phenomenon due to a subluxated stapes foot plate),
hypertropia of one eye (lesion is in the dorsolateral
medulla oblongata), and simultaneous hypertropia
of one eye and hypotropia of the other eye (lesion
is in the midbrain tegmentum).31 The ParksBielschowsky three-step test is commonly used to
differentiate between these two conditions. The first
step should determine which eye is hypertropic in
the primary position (the uncovered eye moves
down as the other is covered). The second step
should focus on whether the hypertropia increases
on right or left gaze, while the third step serves to
determine whether the hypertropia increases on
right or left head tilt. For clinical purposes, we
further divide it according to eye deviation in each
lateral field of gaze: comitant (deviation stays the
same in each lateral field of gaze); incomitant
(hyperdeviation increases in one lateral field of
gaze); and laterally alternating skew deviation
(hyperdeviation of the abducting eye in each lateral
field of gaze).5
In some cases, skew deviation can clinically mimic
trochlear nerve lesion (especially in the case of laterally alternating skew deviation, which can be difficult to distinguish from bilateral fourth nerve
lesion), and it could be difficult to differentiate
between these two conditions. In the first case,,
other focal neurological signs (astasia, dysarthria,
dysmetria) can be present and brain magnetic resonance imaging (MRI) usually reveals a posterior
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Skew Deviation and Ocular Tilt Reaction

3

fossa lesion. This is usually not the case with unilateral peripheral trochlear nerve palsy.5
Indirect ophthalmoscopy and optical coherence
tomography (OCT) retinal nerve fiber layer plots
were found to be useful in objectively quantifying the
degree of ocular cyclotorsion. While in a trochlear
nerve lesion the fundus of the hypertropic eye is excyclorotated, in skew deviation it is incyclorotated and
the fundus of the hypotropic eye is excyclorotated.32 In
both trochlear nerve lesion and skew deviation, the
head is usually tilted contralateral to the side of the
hypertropic eye. In the first case, this represents a
compensatory mechanism (to minimize hypertropia),
while, in skew deviation, it reflects an underlying
pathologic mechanism where it strives to realign the
eyes and head to a tilted position which the brain
perceives as vertical.5,7 Thus, skew deviation is associated with a tilt in the subjective visual vertical; i.e., a
misconception of vertical.3 This is a basis of the
upright-supine test, which is highly specific in differentiating skew deviation from other causes of vertical
strabismus.33 It is thought that, when changing from
an upright to a supine position, the orientation of the
utricles changes from earth-horizontal to earth–vertical, this leads to a saturation or reduction in the overall
afferent activities of the utriculo-ocular reflex, minimizing any asymmetry of the reflex. This leads to the
reduction of torsion and vertical misalignment in skew
deviation. The test is considered to be positive if vertical deviation decreases by ≥50% from the upright to
supine position.5
The ocular tilt reaction and skew deviation
usually resolve spontaneously over weeks to
months.7 As symptomatic relief, an eye patch and
prism may be used. Botulinum toxin and surgical
correction are usually effective in more resistant,
long-term cases.34–36

the patient fell to the left side and, while performing a
tandem walk, a drift to the left was detected.
Movements in the horizontal axis were intact, while
the patient could not perform vertical version and
convergence. The Hess-Lancaster test showed superior
rectus muscle and inferior obliquus muscle palsy on
the left and rectus inferior muscle palsy and superior
obliquus muscle palsy on the right. The ParksBielschowsky three-step test was negative. A cover
alternating test was + from vertical, R/L. Examination
of the ocular fundus showed incyclotorsion of the elevated right eye and excyclotorsion of the depressed eye.
An upright-supine test was positive.
A brain MRI revealed a small zone of diffusion
restriction in the medial portion of the right cerebral
peduncle and right thalamus, consistent with
impaired posterior cerebral artery irrigation and
acute ischemia, as well as diffuse chronic postischemic lesions periventricular, sub-cortically, and in
the brainstem. A previous MRI performed between
hospitalizations found only chronic vascular lesions
supra and infratentorially.
Transcranial doppler (TCD) ultrasonography
revealed no significant changes in haemodynamics
(stenosis/vasospasm), other than diffuse atherosclerotic changes consistent with age.
An electrocardiogram (ECG) as well as Holter
monitor (24 h) detected sinus rhythm and showed
non-specific T-wave abnormalities as well as periodical arrhythmias with three isolated supraventricular
extrasystoles (SVES). The echocardiography did not
disclose a cardiac source of emboli. There was a partial, gradual improvement in the patient’s neurological
status following treatment.
On a regular follow-up visit (two months after hospital discharge), the patient did not report any visual
disturbances, and OTR recovered spontaneously, with
normal neurological examination.

CASE REPORT

DISCUSSION

A 59-year-old man with a long history of high blood
pressure and hyperlipidemia, who previously suffered
an ischemic brainstem stroke, presented with sudden
onset of diplopia, speech disturbances, and gait
impairment (drift to the left). He denied having any
changes of visual acuity, eye pain, or recent trauma.
Neurological examination revealed dysarthria, and a
slightly tilted head towards the left shoulder with lowering of the chin. The right eyeball was positioned
more upwards compared to the somewhat lowered
left eye (vertical misalignment–strabismus). It fell
behind when the patient was requested to look downwards and laterally, whereas the left eye fell backwards when the patient was requested to look
upwards and laterally. The patient complained of
diplopia in any gaze direction. In the Romberg test,

We present a patient who developed sudden-onset OTR:
right-sided skew deviation, head tilt to the left shoulder,
and tilt of the subjective visual vertical. The Parks threestep test was negative and the upright supine test was
positive. One must bear in mind the possibility that OTR
mimics, for example, a trochlear nerve lesion when examining patients who present with head tilt and eye vertical
misalignment, in which the Parks-Bielschowsky threestep test is usually positive, the fundus of the hypertropic
eye excyclorotated, and the upright-supine test is
negative.5 In our patient, fundoscopy showed incyclotorsion of the elevated right eye and excyclotorsion of the
depressed eye, which corroborates skew deviation as an
underlying mechanism. Furthermore, the upright supine
test was positive. A brain MRI revealed a small zone of
diffusion restriction in the medial portion of the right

© 2016 Taylor & Francis

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K. I. Tudor et al.

cerebral peduncle and right thalamus, which is consistent
with clinical presentation. Other neurological signs (dysarthria, ataxia) are suggestive of skew deviation as an
underlying pathological mechanism of vertical
misalignment.5
Finally, symptoms usually resolve spontaneously
(over weeks to months), as was the case with the
presented patient.7

DECLARATION OF INTEREST

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The authors report no conflicts of interest with this
study. The authors alone are responsible for the content and writing of this article.

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