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Esophoria or esotropia in adulthood: a sign of cerebellar dysfunction?

Article  in  Journal of Neurology · December 2014

DOI: 10.1007/s00415-014-7614-2

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J Neurol (2015) 262:585–592
DOI 10.1007/s00415-014-7614-2
ORIGINAL COMMUNICATION
Esophoria or esotropia in adulthood: a sign of cerebellar
dysfunction?
Katharina Hüfner • Claudia Frenzel • Olympia Kremmyda • Christine Adrion
Stanislavs Bardins • Stefan Glasauer • Thomas Brandt • Michael Strupp
Received: 9 September 2014 / Revised: 7 December 2014 / Accepted: 9 December 2014 / Published online: 19 December 2014
Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Convergent strabismus is a common diagnosis
in early childhood, when it is mostly considered benign. If
it develops later in life, strabismus can, however, be a sign
of neurological disease. In these cases the underlying
pathophysiological mechanisms are largely unknown. In
this retrospective case–control study we analyzed the
neuro-ophthalmological examination reports of 400 adult
patients who presented at the German Center for Vertigo
and Balance Disorders to determine an association between
ocular misalignment and cerebellar dysfunction. Patients
with cerebellar signs (i.e., cerebellar ataxia and/or cere-
bellar ocular motor signs) had a 4.49 (95 % CI [1.60;
13.78]) times higher frequency of ocular misalignment and
K. Hüfner
C. Frenzel
O. Kremmyda
M. Strupp
Department of Neurology, University Hospital Munich,
Ludwig-Maximilians University, Campus Grosshadern,
Munich, Germany
K. Hüfner
O. Kremmyda
C. Adrion
S. Bardins

S. Glasauer
T. Brandt
M. Strupp
German Center for Vertigo and Balance Disorders, University
Hospital Munich, Ludwig-Maximilians University, Campus
Grosshadern, Munich, Germany
K. Hüfner (&)
Department of Psychiatry, Medical University of Innsbruck,
Innsbruck, Austria
e-mail: katharina.huefner@uki.at
C. Adrion
Institute for Medical Informatics, Biometry und Epidemiology,
University Hospital Munich, Ludwig-Maximilians University,
Campus Grosshadern, Munich, Germany
S. Glasauer
T. Brandt
Institute for Clinical Neurosciences, University Hospital
Munich, Ludwig-Maximilians University, Campus Grosshadern,
Munich, Germany
•
specifically a 13.3 (95 % CI [3.80; 55.73]) times increased
frequency of esophoria/esotropia (ESO) during distant gaze
than patients without cerebellar dysfunction. ESO when
looking into the distance was associated with saccadic
smooth pursuit, dysmetria of saccades, and downbeat
nystagmus (DBN) (v2 test, p \ 0.0001 for all associations).
Patients with cerebellar dysfunction also showed mildly
impaired eye abduction (v2 test, left eye and right eye:
p \ 0.0001), associated with horizontal gaze-evoked nys-
tagmus (v2 test, p \ 0.0001). The association of ESO and
DBN implicates a pathophysiological involvement of the
cerebellar flocculus, while the association with dysmetric
saccades suggests involvement of the oculomotor vermis.
This is compatible with animal studies showing that the
pathways of the flocculus/posterior interposed nucleus and
vermis/nucleus fastigii are both involved in vergence
movements and static binocular alignment. From a clinical
point of view, a newly diagnosed esophoria/esotropia only
during distant gaze may be a sign of a cerebellar disease.
Keywords Esophoria
Esotropia
Distant gaze

Cerebellar dysfunction
Introduction
Strabismus is frequently found in young children, in whom
its prevalence is between 2 and 5 % [10, 31]. The two
major categories of early onset concomitant esotropia are
accommodative and congenital (infantile). In concomitant
strabismus the ocular deviation does not vary with direc-
tion of gaze as opposed to incomitant forms. While there is
some disagreement on the exact pathophysiology of these
strabismus disorders, there is a general consensus that they
are not as a rule causally related to any serious underlying
123
586
neurological pathology, even if the onset is sudden [13, 31,
41]. Subtle cases can go undiagnosed, becoming apparent
in adult life when an affected individual experiences stress,
a minor head trauma, or fatigue. All can lead to the
decompensation of a previously latent strabismus and the
sudden onset of diplopia.
In cases when new ocular misalignment develops in
adulthood, it is usually incomitant (i.e., varies with
direction of gaze) and caused by a defined and localized
neurological or ophthalmological disease such as cranial
nerve palsies, brainstem pathologies or disease of the
ocular muscles. A few case reports, case series, and
commentaries have described the appearance of a new
acute comitant esophoria/esotropia, which is larger when
looking into the distance, in later childhood or adulthood
in patients with cerebellar disease such as cerebellar
tumors, including astrocytomas and medulloblastomas as
well as Arnold–Chiari I malformations [13, 32, 37, 43].
Acquired esophoria/esotropia can be associated with other
eye movement abnormalities, such as dysmetric saccades,
gaze-evoked nystagmus, or downbeat nystagmus (DBN)
[40]. After initially successful surgery for strabismus,
patients with Arnold–Chiari malformation can also
develop recurrent esotropia with diplopia, which resolves
upon suboccipital decompression [8, 32]. Esotropia can
also be caused by acute lesions of the thalamus [9] and the
corpus callosum [1]. Finally, vertical misalignment of the
eyes has also been described in patients with cerebellar
disease [12].
In this retrospective case–control study we investigated
whether there is a higher frequency of ocular misalignment,
namely concomitant esophoria/tropia, in patients with
cerebellar dysfunction than in patients without cerebellar
symptoms, in order to evaluate the co-occurrence of these
conditions in an adult patient population.
Methods
Neuro-ophthalmological and orthoptic examination
All subjects underwent a standardized neurological and
neuro-ophthalmological examination at the German Center
for Vertigo and Balance Disorders at the University Hos-
pital Munich, Campus Grosshadern, between 1999 and
2009 as described previously (e.g., [14]). The following
parameters were evaluated in the present study and
dichotomised for statistical analysis: patient ID, age (in
years), neurological diagnosis, control/patient status, pre-
sence of saccadic smooth pursuit (yes/no), downbeat nys-
tagmus (yes/no), pathological vestibulo-ocular reflex
(VOR) by the head-impulse test (yes/no), saccadic dys-
metria (yes/no), rebound nystagmus (yes/no), gaze-evoked
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J Neurol (2015) 262:585–592
nystagmus (yes/no), visual fixation suppression of the VOR
(normal/abnormal), motility of right and left eye during
abduction in mm (0–10) [20], ocular alignment when
looking at a near target and into the distance as well as
during lateral gaze into the distance (i.e., orthophoria/eso
deviation/exo deviation/vertical deviation/congenital stra-
bismus), ocular motility (i.e., intact/abduction deficit/
abducting hypertropia). Observation of the fundus and
fundus photography using a scanning laser ophthalmoscope
was done online and the subjective visual vertical was also
determined.
Additional examinations were performed in all cere-
bellar patients in order to uncover underlying causes of the
cerebellar disease. These included caloric irrigation
(n = 136), cranial MRI (n = 136), laboratory examina-
tions, including CSF (n = 38), laboratory examinations,
excluding CSF analysis (n = 78).
Study population
A total of 400 subjects who presented with vertigo, dizzi-
ness or unsteadiness of gait at the German Center for
Vertigo and Balance Disorders at the University Hospital
Munich were included in the retrospective case control
study. 199 of the participants had a known or newly
diagnosed cerebellar dysfunction and were termed the
cerebellar group (CBL). Patients with localized cerebellar
or cerebral disease such as infarction, tumor or demyelin-
ation were not included. Cerebellar dysfunction included
cerebellar ataxia [ataxia of stance (n = 67), ataxia of gait
(n = 86), ataxia of speech (n = 33) and limb ataxia/dys-
diadochokinesis/dysmetria/rebound phenomenon (n = 73)]
and/or ocular motor cerebellar signs (all patients). Data on
additional cerebellar signs were not available for 14 CBL
patients. A specific etiology was identified in 68 of the
CBL patients: cerebellar ataxia and bilateral pathological
head-impulse test ± polyneuropathy syndrome ([22],
n = 31) spinocerebellar ataxia (n = 9), episodic ataxia
(n = 9), inflammatory or toxic (n = 7), multiple system
atrophy (n = 3), Arnold–Chiari I (n = 3), miscellaneous
known etiologies (n = 6); 131 had a degenerative cere-
bellar disease of unknown etiology. All patients with
tropias complained of double vision. The CBL group was
compared to an age- and gender-matched group of 201
control patients ‘‘CON’’ (age CBL: 66.3 ± 13.9 years
(mean ± SD), CON: 67.1 ± 14.5 years; p = 0.57 and sex
ratio CBL: 85 females, CON: 91 females) who, just as the
cerebellar patients, had a leading symptom of vertigo,
dizziness or unsteadiness of gait. The control patients
(bilateral vestibulopathy, Menière’s disease, benign par-
oxysmal positioning vertigo and vestibular migraine)
underwent the same neurological and neuro-ophthalmo-
logical examinations as the CBL.
J Neurol (2015) 262:585–592 587

Statistical analysis Table 1 Oculomotor findings in patients with cerebellar dysfunction

and controls
Statistical analyses included frequency and descriptive Oculomotor CBL patientsa CON patientsa
statistics. v2 or Fisher’s exact test was applied to compare findings
proportions. Logistic regression adjusting for possible
Saccadic smooth pursuit
confounders (e.g., saccadic smooth pursuit, saccadic dys-
Yes 193/199 51/201
metria, rebound nystagmus, disturbed fixation suppression,
No 6/199 150/201
and gaze-evoked nystagmus) was applied to compare the
Downbeat nystagmus
prevalence of a certain disorder of ocular alignment in the
Yes 137/199 0/201
cerebellar vs. control group. Statistical analyses were per-
No 62/199 201/201
formed using RÒ software package version 2.11.1 (http://
Bilaterally pathological head-impulse test
www.r-project.org). All reported statistical tests were two
Yes 71/199 86/201
sided, and the significance level was set to 5 %.
No 128/199 115/201
Videooculography (VOG) recordings Saccadic dysmetria
Yes 73/199 8/201
A dataset from a selected cerebellar patient was recorded No 126/199 193/201
using binocular videooculography (EyeseecamÒ). The Rebound nystagmus
VOG system consists of two cameras fixed on a head band. Yes 64/199 1/201
The patient had to fixate on a central target located either No 135/199 200/201
30 cm (near target paradigm) or 4 m (distant target para- Gaze-evoked nystagmus
digm) away, during alternating monocular fixation (alter- Yes 185/199 31/201
nating cover test). The head rested on a chin rest. No 14/199 170/201
Visual fixation suppression of VOR
Abnormal 147/199 2/201
Results Intact 52/199 199/201
Abduction RE in 9.34 ± 1.00 (per 9.97 ± 0.27 (per
Disturbances in ocular alignment of patients mmb 199) 201)
with cerebellar dysfunction Abduction LE in 9.30 ± 1.05 (per 9.95 ± 0.40 (per
mmb 199) 201)
ESO distant gaze straight ahead and/or lateral gaze
The following factors were analyzed in the described
Yes 122/198 8/201
models: ESO included the factors esotropia (ocular con-
vergence during binocular view) and esophoria (ocular No 76/198 193/201
convergence during monocular view); EXO included the VD distant gaze straight ahead and/or lateral gaze
factors exotropia (ocular deviation during binocular view) Yes 48/195 7/201
and exophoria (ocular deviation during monocular view); No 147/195 194/201
VD (vertical deviation) included VD (left eye over right Ocular alignment distant gaze straight ahead
eye) and ?VD (right eye over left eye) (see Table 1 for Orthophoria 83/198 177/201
exact numbers). Vertical divergence did not include any ESO 95/198 5/201
other features of skew deviation or isolated nerve/muscle EXO 9/198 14/201
palsies. VD 9/198 3/201
In a first, exploratory analysis, the presence of abnor- CS 2/198 2/201
malities of ocular alignment (ESO, EXO, VD) was deter- Deviation angle distant gaze straight ahead in degreeb
mined in CBL vs. CON during gaze straight ahead in the ESO 2.0 ± 1.8 (per 90) 1.8 ± 0.8 (per 5)
distance. In a bivariate analysis, anomalies in ocular Deviation angle lateral gaze in the distance in degreeb
alignment during gaze straight ahead in the distance were ESO 3.3 ± 1.9 (per 110) 2.0 ± 0.8 (per 6)
more prevalent in the CBL group than in the CON group Ocular alignment near gaze straight ahead
(v2 test, p value \0.0001). A logistic regression model Orthophoria 21/188 24/200
adjusting for saccadic smooth pursuit, rebound nystagmus, ESO 15/188 1/200
disturbed visual fixation suppression of the VOR, and gaze- EXO 144/188 170/200
evoked nystagmus, revealed an estimated odds ratio (OR) VD 6/188 3/200
of 4.49 for CBL vs. CON (95 % CI [1.60; 13.78]). Hence, CS 2/188 2/200
CBL had a 4.49 times increased risk of displaying

123
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Table 1 continued
Oculomotor CBL patientsa CON patientsa
findings
Ocular motility
Normal 79/199 193/201
Abduction deficit 64/199 5/201
Abducting 34/199 3/201
hypertropia
Abduction deficit 22/199 0/201
plus abducting
hypertropia
CBL cerebellar, CON control, VOR vestibulo-ocular reflex, ESO
esophoria/esotropia, EXO exophoria/exotropia, VD vertical deviation,
CS congenital strabismus, RE right eye, LE left eye
a
The number of analyzed cases for each coding is indicated
b
Mean of all analyzed cases ± standard deviation, the number of
analyzed cases is given in brackets
abnormalities in ocular alignment during gaze straight
ahead in the distance (p = 0.005). When disturbances in
ocular alignment (EXO, ESO, VD) were determined during
near fixation no statistically significant association was
found with the presence of a cerebellar dysfunction (v2 test,
p = 0.916). This finding was confirmed using logistic
regression (CBL vs. CON group: OR = 0.84; 95 % CI
[0.208; 3.576]).
Esophoria/esotropia, exophoria/exotropia
during near and distant gaze in cerebellar dysfunction
A significant association of ESO during gaze straight ahead
in the distance and cerebellar dysfunction was detected (v2
test, p \ 0.0001). This association was also found during
lateral gaze (v2 test, p \ 0.0001) and was confirmed using
logistic regression adjusting for possible confounders
(smooth pursuit, rebound nystagmus, visual fixation sup-
pression of the VOR, and gaze-evoked nystagmus)
(p = 0.0001). The risk for ESO during gaze in the distance
was 13.3 times higher in the CBL than in the CON group
(95 % CI [3.80; 55.73]). No association of ESO during
near fixation and cerebellar dysfunction was found (v2 test,
p = 0.709). No significant association between ESO dur-
ing near fixation and during distant gaze was found (v2 test,
p = 0.897). This reveals that patients exhibiting esophoria
or esotropia during distant gaze do not tend to show eso-
phoria or esotropia during near gaze. Binocular eye
movement recordings (horizontal traces) were performed
in a representative patient with cerebellar disease to visu-
alize the occurrence of ESO alignment during distant but
not during near gaze (Fig. 1). There was no evidence for an
association between EXO during gaze straight ahead in the
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J Neurol (2015) 262:585–592
distance and the presence of cerebellar dysfunction (v2 test;
p = 0.100).
Vertical deviation and cerebellar dysfunction
In a bivariate analysis a significant association between
vertical deviation during gaze in the distance and cerebellar
dysfunction was found (v2 test, p \ 0.0001). There was
also an association between the occurrence of vertical
deviation and saccadic smooth pursuit (v2 test, p \ 0.0001)
and DBN (v2 test, p \ 0.0001), respectively.
Impairment of ocular motility in patients
with cerebellar dysfunction
The presence of disturbances in ocular motility (abducting
hypertropia or disturbance in ocular abduction) was more
frequent in the CBL patients than in the CON (v2 test,
p \ 0.0001). Ocular motility\10 mm during abduction was
considered pathological, while 10 mm or more was con-
sidered normal [20]. A significant association between
pathological ocular motility during eye abduction and cer-
ebellar dysfunction was found in a bivariate analysis (v2 test,
left eye: p \ 0.0001, right eye: p \ 0.0001). Patients with
deficits in eye abduction were found to also have horizontal
gaze-evoked nystagmus (v2 test, p \ 0.0001). When only
the ocular motility of the right eye was considered for
analysis, a significant association between the reduced eye
abduction in mm and horizontal gaze-evoked nystagmus
was found (v2 test, p \ 0.0001). This was confirmed using a
Cochran–Armitage trend test for proportions to explore the
association between pathological eye abduction and the
occurrence of gaze-evoked nystagmus (p \ 0.0001).
Esophoria/esotropia and cerebellar ocular motor
disturbances
To test for a possible abduction deficit as the cause of ESO
in the distance, the presence of ESO during lateral gaze
was investigated to determine if it was associated with
gaze-evoked nystagmus. A significant association of the
two parameters was found (v2 test, p \ 0.0001). ESO in the
distance was also associated with saccadic smooth pursuit
(v2 test, p \ 0.0001) and saccadic dysmetria (v2 test,
p \ 0.0001). Patients with DBN were more frequently
affected with ESO during distant gaze than patients without
DBN (v2 test, p value \0.0001).
Subjective visual vertical in patients with esophoria/
esotropia
ESO in the distance or nearby was not associated with a
displacement of the subjective visual vertical in our
J Neurol (2015) 262:585–592
Fig. 1 Binocular eye movement recordings (horizontal traces) from
a patient with cerebellar dysfunction. Cover tests during far (4 m) and
near (30 cm) fixation are shown. Positive values indicate movement
to the left. Traces for right eye (RE gray lines) and left eye (LE black
lines) are shown. ESO (here of about 7°) is visible only during distant
patients (Fisher test: p = 0.529 and p = 0.086
respectively).
Discussion
The major finding of the current study is that cerebellar
dysfunction is associated with distant esophoria/esotropia
in adulthood. Second, esophoria/esotropia is associated
with mildly impaired ocular motility, specifically eye
abduction. Third, further ocular motor signs of cerebellar
dysfunction co-occurred with esophoria/esotropia. Fourth,
the statistically significant association of ESO with DBN
points to a possible pathophysiological involvement of the
cerebellar flocculus, while the association with saccadic
dysmetria suggests involvement of the oculomotor vermis.
The flocculus of primates contains neurons that dis-
charge with the angle of vergence [28] and ablation of the
cerebellum can lead to paralysis of vergence [42]. Exper-
iments in rodents have shown that stimulation of floccular
Purkinje cells can cause abduction of the ipsilateral eye [7]
589
fixation, as indicated by the re-fixation saccade towards the direction
of the fixating eye (e.g., movement to the left, during left eye fixation
or else right eye cover). In near fixation, there is no occurrence of re-
fixating eye movements during the cover test (notice that both eyes
are adducted about 7°, due to convergence)
and that floccular signals inhibit the medial rectus and
excite the lateral rectus muscle [15]. Stimulation of the
cerebellar flocculus can lead to movements of one eye
only, which can be downwards or horizontal [3]. Thus,
dysfunction of the cerebellar flocculus in animal studies
can result in an increased inward tone of the eyes. There-
fore, a likely pathophysiological mechanism of the
observed ESO in patients with cerebellar dysfunction is an
impaired abduction of the eyes due to floccular dysfunc-
tion. This view is supported by the observation that the
esophoria/esotropia was associated with horizontal gaze-
evoked nystagmus and downbeat nystagmus. Our finding
has also been supported by others [40].
Experiments on binocular eye alignment and coordina-
tion in monkeys have shown that the supraoculomotor area,
which is located immediately adjacent to the oculomotor
nucleus in the brainstem and projects monosynaptically to
the medial rectus motoneurons, encodes vergence move-
ments in healthy monkeys [26] as well as a signal related to
the ocular misalignment in monkeys with strabismus [6].
This area is thought to receive input from the caudal
123
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fastigial nuclei (cFN) and the posterior interposed nucleus
(PIN, corresponding to the globose and emboliform nuclei
in humans) in the cerebellum [25]. In one of the few
available animal studies on the etiology of strabismus [18]
cFN inactivation induced an exo (outwards) deviation of
the eyes while PIN inactivation led to an eso (inward) tone
of the eyes. The authors suggested that in esotropia the
cFN/PIN-supraoculomotor area-medial rectus motoneuron
circuit provides a convergence bias signal to the medial
rectus muscle. The abducens nucleus must also receive
these signals to allow for relaxation of the lateral rectus
[19]. The reason for these erroneous signals remained
unclear in the aforementioned studies. Experimental
removal of the oculomotor vermis in monkeys led to,
among other oculomotor disturbances, esodeviation of the
eyes and disturbances in phoria adaptation [38]. This could
be related to a disruption of the cFN-supraoculomotor area-
medial rectus motoneuron circuit described above, since, in
animal experiments, the oculomotor vermis has been
shown to project to and inhibit the cFN [44], while the PIN
is anatomically connected to the flocculus [39].
In agreement with these findings, patients with cere-
bellar lesions exhibit reduced divergence but not conver-
gence velocity to ramp targets. These defects were
particularly evident in patients with vermal lesions [36].
Functional imaging studies in humans have shown activa-
tion of the cerebellar vermis and hemispheres during the
near response [35]. Esotropia with greater esodeviation at
distance was described in patients with lesions to the dorsal
cerebellar vermis [30]. The pathogenetic significance of the
vestibulo-cerebellum in maintaining correct ocular align-
ment is underscored by case reports describing periodic
alternating nystagmus, attributed to lesions in the vestibu-
lo-cerebellum, in combination with alternating vertical
misalignment of the eyes [33].
Both the floccular and also the vermal pathways possi-
bly play a role in maintaining the correct static binocular
alignment. It has been proposed that the floccular/PIN
pathway may be involved in the control of divergence eye
movements, while the dorsal vermis/cFN pathway may be
more related to convergence, but such compartmentaliza-
tion of functions remains a hypothesis [21]. These findings
fit well with the results of our present study, which iden-
tified the reduced ocular abduction and associated hori-
zontal gaze-evoked nystagmus as the probable mechanism
of esophoria/esotropia in patients with cerebellar
syndrome.
Many types of oculomotor adaptation require an intact
cerebellum for their normal performance [17, 24]. Patients
with cerebellar lesions were shown to have significantly
reduced horizontal phoria adaptation [27]. However, this
could not be confirmed in a different study [11]. This
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J Neurol (2015) 262:585–592
discrepancy might be explained by the fact that in the latter
study base-out prisms were used, which elicited a conver-
gence response. The convergence reaction is not impaired
in patients with cerebellar lesions. These patients, on the
contrary, show ‘‘too much’’ convergence and thus esotro-
pia/esophoria. This might explain why patients with cere-
bellar lesions can be found to have disturbed horizontal
phoria adaptation when base-in prisms are used and intact
adaptation when base-out prisms are used. Phoria adapta-
tion to vertical binocular disparity is frequently impaired in
patients with cerebellar dysfunction [23]. Unfortunately,
fusional abilities were not measured in the current study.
Also vertical misalignment was observed in patients
with cerebellar lesions. It was previously termed ‘‘incom-
itant skew’’ or ‘‘abducting hypertropia’’. We prefer the
latter term, since a true skew deviation is usually part of the
ocular tilt reaction, which was not present in our patients. It
has, however, been observed that true skew deviation,
including SVV deviation, cyclorotation, and vertical devi-
ation can be observed in patients with localized cerebellar
lesions, which mainly include the dentate nucleus [2]. In
our patients, the vertical misalignment changed with the
direction of view, i.e., the deviations often showed a
characteristic pattern of alternating skew deviation on right
and left lateral gaze with the abducting eye higher
(described before [40]). It is possible that otolith influences
and their cerebellar processing play a role in the ocular
misalignment observed in cerebellar patients. Lesions to
the uvula, nodulus and flocculus influence the processing of
vestibular information. Especially the otolith influences
might be important for the observed effects [4].
However, not all cases of adult onset esophoria/esotro-
pia during gaze in the distance are related to cerebellar
disease. The term ‘‘divergence insufficiency esotropia’’ has
been used to describe idiopathic cases in older adults as
well as cases associated with neurological disorders such as
pseudotumor cerebri or progressive supranuclear palsy [16,
34], while ‘‘age-related distance esotropia’’ or ‘‘sagging
eye syndrome’’ describe cases caused by an involutional
effect of orbital connective tissue degeneration [5, 29]. In
our opinion these different terms describe the identical
clinical syndrome which can be caused by a variety of
underlying pathologies, one of which we propose to be
cerebellar dysfunction.
The present study has inherent limits which are due to
the retrospective and cross-sectional approach. The study
design did not allow for a follow-up of patients. Until
prospective, longitudinal data are available we would like
to propose a practical clinical approach: In patients with a
newly diagnosed esotropia/esophoria during gaze only in
the distance, a further neurological evaluation for a cere-
bellar dysfunction should be performed.
J Neurol (2015) 262:585–592
Acknowledgments This study was not industry sponsored. The
study was supported by the German Federal Ministry of Education
and Research (BMBF 01EO0901). We thank Judy Benson and Katie
Ogston for carefully copy-editing the manuscript.
Conflicts of interest None declared.
Ethical standard The study was approved by the ethics com-
mittee of the Ludwig-Maximilians University, Munich, Germany
and was performed in accordance with the ethical standards laid
down in the 1964 Declaration of Helsinki and its later amend-
ments. Written informed consent was obtained for the videoocu-
lography recordings.
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