Definition

Vertical strabismus describes a vertical misalignment of the eyes. By convention, the misalignment is typically labelled by the higher, or hypertropic, eye. The vertical misaligned can also be labelled by the lower, or hypotropic eye.^[2] Some advocate labelling vertical misalignments based on if the deviated eye manifests as a hypertropia or hypotropia. Depending on which eye is fixing, a hypertropia of one eye is the same as a hypotropia of the fellow eye. If the degree of deviation in all fields of gaze, it is classified as comitant; it if behaves differently in different fields of gaze, it is classified as incomitant.

Etiology

Vertical misalignments of the eyes typically results from dysfunction of the vertical recti muscles (inferior and superior rectus) or of the oblique muscles (the inferior oblique and superior oblique). More rarely, they are caused by abnormal positioning of the horizontal rectus muscles. Muscle disfunction may result from paresis, restriction, over-action, muscle malpositioning, and dysinnervation.

Due to muscle restriction or over-action

Thyroid Eye Disease

Thyroid eye disease leads to enlargement of the extraocular muscles and restrictive strabismus. Although any extra-ocular muscle can be involved, the inferior rectus is the most frequently affected, followed by the medial rectus muscle .^[2]^[3]

Associated findings include: Intraocular pressure may increase when looking away from the restriction, ^[4]^[2] proptosis, lid retraction, compressive optic nerve dysfunction, conjunctival hyperemia, chemosis, and corneal affections due to exposure^[5]^[6]^[7]

Brown Syndrome

Poor movement of the superior oblique tendon through the trochlea leads to limited elevation of the eye in adduction, frequently with an associated exotropia in upgaze.

Cause:^[4]^[8]^[9]^[10]^[11]^[12]^[13]^[14]

Congenital (Ex.: Inelasticity of the SO muscle-tendon complex; pseudo-Brown's syndrome due to inferior orbital adhesions; inferior displacement of the lateral rectus). A spontaneous resolution of congenital Brown’s syndrome has been reported.^[15]^[16]
Iatrogenic (Ex.: Following glaucoma, oculoplastics or strabismus surgery; ENT surgery)
Inflammation of the trochlea (Ex.: Rheumatoid arthritis; systemic lupus erythematosus)
Traumatic
Nasal sinus infection
Tight superior oblique muscle (Ex.: Thyroid ophthalmopathy; secondary to superior oblique overaction)
Neoplastic
Hurler-Scheie syndrome
Idiopathic

Inferior Oblique Overaction

Over-elevation of the eye in adduction

Other features: If primary and bilateral, it gives rise to a Y-pattern, with divergence in upgaze; if secondary, i.e. due to a paresis of another vertical muscle, it may give rise to a V pattern, with additional convergence in downgaze. When it is primary (not related to a paresis of another vertical muscle), the head tilt- test is negative (the superior rectus and oblique muscles are ‘’working’’).^[4]

It is frequently bilateral and associated with a horizontal strabismus, although it may be isolated.

Causes:

Primary
Secondary to an ipsilateral superior oblique paresis or a contralateral superior rectus paresis.

Superior Oblique Overaction

Vertical deviation, that increases on adduction of the affected eye. Ex.: A left superior oblique overaction causes a right hypertropia on right gaze.

Other features: Intorsion and abduction in downgaze. If congenital, the intorsion is frequently only objective and not subjective, since there is sensory adaptation. It frequently coexists with an underaction of the contralateral IR and intermittent exotropia. Sometimes it can give rise to an acquired Brown’s syndrome, due to SO contracture (for the differential diagnosis between SO overaction and Brown’s syndrome, see the differential diagnosis section).^[4] A vertical deviation in primary position is more frequently associated with a unilateral or asymmetric SO paresis.^[2] When bilateral, it frequently gives rise to lambda-pattern, with accentuated exotropia in downgaze.^[4]

It is more frequently bilateral. It often coexists with an intermittent exotropia or other forms of horizontal strabismus.

Causes:

Primary
Secondary to a contralateral inferior rectus paresis.

Orbital Causes of Vertical Restriction

Orbital wall fracture with entrapment, orbital mass, and orbital or extraocular muscle inflammation can lead to vertical strabismus

Due to a weak muscle

Unilateral Superior Oblique Paresis

Hypertropia that increases on adduction and and with ipsilateral head tilt. Ex.: Left superior oblique paresis causes a left hypertropia on right gaze and head tilt to the left.

It is the most common cause of an isolated vertical deviation.^[4]^[17]

Other features: Mild extorsion (<10º); compensatory head tilt to the contralateral side and face turn towards the contralateral shoulder, sometimes associated with a facial asymmetry; contralateral inferior rectus overaction (“fallen eye’’)^[4]; large vertical fusional amplitudes when congenital.^[4]^[2]

Causes: ^[4]^[18]^[19]^[20]^[21]

Congenital and traumatic causes are the most frequent (Congenital causes are frequently due to absent trochlear nerves, muscle hypoplasias or tendon laxity but muscle/tendon agenesis has also been described. Symptoms sometimes arise in late childhood or middle age. If traumatic, it is bilateral until proven otherwise.)

Vascular
Neurologic (ex.: Myasthenia gravis)
Iatrogenic (ex.: Slipped muscle; following tenotomy or tenectomy procedures)
Diabetic mononeuropathy
Neoplastic
Viral (ex.: Herpes zoster)
Nasal sinus affections (ex.: Mucocele)

Bilateral Superior Oblique Paresis

Left hypertropia in right gaze and left tilt, right hypertropia in left gaze and right tilt, the hypertropia is less evident than in unilateral superior oblique paresis.

Other features: Larger extorsion than in unilateral paresis (>10º); esotropia increasing in down gaze (>10º) – V pattern of the ''arrow subtype''.^[4] Sometimes bilateral involvement can be masked due to an asymmetrical involvement. Some signs that can be suggestive of bilateral involvement are the reversal of hypertropia on ipsilateral side gaze and contralateral head tilt^[22], objective fundus extorsion ^[2] and a slight IO oblique overaction of the other eye,^[4]as sometimes it becomes evident only after a surgical correction.^[23]

Causes:^[18]

Trauma (The IV cranial nerves exit the midbrain very closely so that strong head traumas, or sometimes even small ones, frequently origin bilateral rather than unilateral palsies)
Neoplastic
Vascular
Craniosynostosis
Congenital (uncommon)

Superior Rectus Underaction

Leads to an elevation deficit/ vertical misalignment that is worst when the affected eye is abducted and with ipsilateral head tilt.

Causes:^[4]^[24]^[2]^[25]^[26]^[27]

Iatrogenic (ex.: Following superior rectus weakening procedures, glaucoma surgery, oculoplastic surgery, scleral buckle insertion.)
Traumatic
Innervational anomaly of the superior division of the III cranial nerve
Muscle aplasia
Neoplastic (ex.: Pineocytoma, orbital tumor)

Monocular Elevation Deficit Syndrome (MEDS)

Limitation of elevation with contralateral hypertropia, previously called double elevator palsy.

Other features: Chin elevation^[2]and ipsilateral true or pseudo-ptosis.^[28]

Cause: It can have various causes, such as orbital restrictive or neurological causes (supranuclear, nuclear or infranuclear). ^[4]Sometimes it can be associated with congenital inferior rectus restriction, superior rectus palsy ^[29] or both. ^[4]^[30]

Inferior Rectus Underaction

Leads to a depression deficit/ vertical misalignment that is worst when the affected eye is abducted and with contralateral head tilt.

Causes:^[4]^[2]^[31]^[32]^[33]^[34]

Iatrogenic (ex.: Overcorrections following inferior rectus weakening procedures as in thyroid ophthalmopathy )
Traumatic
Innervational anomaly of the inferior division of the III cranial nerve
Muscle aplasia (The inferior rectus is most frequently affected, it can be associated with craniofacial disorders)
Neoplastic
Neurological (ex.: Myasthenia gravis)

Unilateral Inferior Oblique Paresis

Leads to an elevation deficit in adduction and greater vertical deviation with tilt to the contralateral side. It frequently leads to a contralateral hypertropia due to overaction of the yoke muscle (SR). The increase of vertical deviation in adduction and upgaze to the contralateral side. Hypertropia, that increases on head tilt to the contralateral side. Ex.: Left inferior oblique paresis causes a right hypertropia on right and up gaze and head tilt to the right.

It is a rare and a bilateral involvement is very uncommon.

Causes:^[4]^[35]^[36]

Most frequently idiopathic or iatrogenic (following inferior oblique surgery or retrobulbar block).

Congenital
Traumatic
Vascular
Neurological

Myasthenia Gravis

A very rare form of isolated IR affection has been described^[37]

Other complex forms of strabismus or involving multiple muscles

Canine Tooth Syndrome

In addition to the restrictive elevation, there is also a SO paresis. It is frequently traumatic.^[4]

Pseudoinferior Rectus Palsy

Slight hypertropia in primary position as muscular function is preserved from upgaze to primary position, and a large hypertropia from primary position to downgaze. It can be caused by an adherence of the inferior rectus to the orbital floor following a traumatic fracture, giving rise to a muscle slack in front of the adherence. ^[4]

Displaced Horizontal Recti

If horizontal recti are displaced superior- or inferiorly, they act as additional elevators or depressors. V and A patterns may result simulating oblique muscle paresis/overactions.

Causes:^[4]^[38]

Congenital (ex.: Craniosynostosis; extorted orbit)
Iatrogenic (ex.: Following strabismus surgery)
High myopia, where a posterior staphyloma misplaces the lateral rectus inferiorly.

Iatrogenic Strabismus

Frequently due to peri-orbital fat adhesions to the eye globe, leading to a restrictive syndrome (Ex.: pseudo-Brown's syndrome), or following retinal surgery:

Scleral buckle with posterior slippage, entrapment or splitting of extraocular muscles and anterior displacement of an oblique muscle.^[4]^[25]
Following ocular surgery (Ex.: Strabismus surgery; glaucoma surgery, especially with the Baerveldt device or due to a mass effect caused by the bubble^[26]; oculoplastic surgery)^[27]

Duane Syndrome

Sometimes associated with a hypertropia in adduction, due to aberrant innervation of vertical muscles or a restrictive lateral muscle.

Large Angle Exotropia

Hypertropia or hypotropia in in adduction. – X- pattern

It is caused by a tight, contracted lateral rectus. As the eye tries to adduct, it slips below or above the eyeball, causing an upward or downward vertical deviation^[4]^[2]

Congenital Fibrosis of the Extraocular Muscles:

May affect any extraocular muscle, but sometimes affects solely the inferior rectus. It is thought to be related to innervational and structural abnormalities of the extraocular muscles.^[2]^[39]^[40]

Dissociated Vertical Deviation

A dissociated vertical deviation is an upward drift of one eye when binocular fusion is interrupted (such as with alternate cover testing) that is not associated with a compensatory downward shift of the fellow eye when attention if focused on the drifting eye. For example, on alternate cover testing, the right eye would drift upward when covered and be seen to come down when the left eye is covered. When the cover is switched back to the right eye again, there is NO upward refixation movement of the left eye. With a bilateral dissociated vertical deviation, both eyes are seen to drift up when covered and re-fixate with a downward movement when uncovered. It manifests when binocular fusion is interrupted either by occlusion or by spontaneous dissociation.^[4]

Other features: Abduction and extorsion. Increased vertical deviation on head tilt to the ipsilateral side.^[4]

Most frequently both eyes are affected, although it may be asymmetrical . When bilateral, the vertical deviation of each eye is not related to the other, as in true hypertropia (no yoke muscle overaction is present).^[4]^[41]

Cause: Any cause leading to a disruption of normal binocular development can be at its origin. Rarely primary.

Signs and Symptoms

Suppression

Is not perceived by the patient, but rather by the observer. Suppression typically happens when the deviation starts in the early years of life (before 6 years of age), when the neuroplasticity of the visual system is still capable of suppressing the image coming from the deviated eye. The amount of suppression, which can vary from small suppression scotomas in binocular fusion to large suppression areas on the affected side and amblyopia, depends on various factors such as the size of the strabismus and age of onset.

Diplopia

Occurs when the deviation is acquired after a significant maturation of the visual system (7 to 8 years of age), when suppressive mechanisms are usually no longer initiated. Younger children may also have transitory diplopia in acquired forms of strabismus, before suppression kicks in. In the case of a hypertropia, the diplopia is vertical.

Confusion

Two images are perceived in the same location, due to a misalignment of retinal correspondence points on the fovea. This symptom is rare, when compared to diplopia and the same rules apply for age of patients affected. It has been observed in glaucoma patients with an acquired strabismus (see strabismus following glaucoma surgery), due to tunnel vision and forced use of the fovea.

Diagnosis

Sensorimotor Testing

The degree of misalignment should be determined for at least primary, horizontal, and vertical gazes and in head tilt. Torsion can be testing with the double maddox rod test. Haplosopic testing can be performed to evaluate for the ability to fuse in the setting of torsion. Worth 4 dot and Bagolini lenses can be used to evaluate for suppression. Specific methods for testing are detailed in the highlighted link above.

Differentiating between a Paresis and a Restriction of the Antagonist

Forced Duction Test: Forced duction testing can evaluate for evidence of restriction and possibly of laxity in the setting of a muscle palsy

Saccadic Eye Movements: In the case of a restriction, normal saccadic eye movements can be observed until the full restrictive amplitude is achieved, where it stops abruptly. In the case of a palsy, saccadic velocity and force generation are decreased

Intraocular Pressure: Restrictions may lead to increase IOPs when the eye is moving against the restriction.

Lid fissure: Restrictions may cause lid fissure narrowing, while a paresis causes lid fissure widening.^[4]

Three Step Test for Cyclovertical Muscle Palsy

The Parks-three-step-test can be used to help determine the cause of a vertical misalignment caused by a single muscle paresis. The superior rectus and inferior oblique muscles elevate the eye and the inferior rectus and superior oblique muscles depress the eye. When the head is tilted, extorsion and intorsion movements are executed. The superior oblique and superior rectus muscles are intortors and the inferior oblique and inferior rectus muscle are extorters. The oblique muscles abduct the eye and the vertical recti muscles adduct the eye. However, oblique muscles have the greatest effect on vertical alignment when the eye is adducted and so are tested in adduction. The ability of the vertical recti muscles to elevate/ depress the eye is testing in abduction.

Cardinal positions of gaze

Determine which eye is hypertropic
1. The impacted muscle will be a depressor of the higher eye (inferior rectus or superior oblique) or a elevator of the lower eye (superior rectus or inferior oblique)
Determine in which horizontal gaze the hypertropia is worse
1. If worse in left gaze, the oblique muscles in the right eye or the vertical recti in the left eye are affected
2. If worse in right gaze, the oblique muscles in the left eye or vertical recti in the right eye are affected
Determine in which head tilt the deviation is the worse
1. If worse in right tilt, the right eye intorters (superior oblique and superior rectus) or left eye extorters (inferior oblique and inferior rectus) are affected
2. If worse in left tilt, the left eye intorters (superior oblique and superior rectus) or right eye extorters (inferior oblique and inferior rectus) are affected
  
  3 Step Test Showing Right Superior Oblique Palsy

Tip: You can draw the cardinal positions of gaze as above and circle: 1) the bottom muscles on the higher eye and top muscles on the lower eye, 2) the muscles to the patient's right in both eyes if worse in right gaze or to the patient's left in both eyes if worse in left gaze, 3) the muscles in line with whichever direction the head tilt is worse. In the right superior oblique example to the right, the right eye is hypertropic and the deviation is worse in left gaze and right tilt.

The tree-step-test is not diagnostic when more than one muscle is affected or there is a restrictive cause; there are some situations where a false positive result can lead to a misdiagnosis: A paresis of more than one vertical muscle, contracture of the vertical recti, previous vertical muscle surgery, skew deviation, myasthenia gravis, dissociated vertical deviation and small vertical deviations associated with horizontal strabismus.^[42]

Differentiating between Brown’s Syndrome, Superior Oblique Overaction and Inferior Oblique Paresis

Patients with Brown’s syndrome will have a positive forced-duction test especially evident on the Guyton’s exaggerated forced-duction test. In Brown’s syndrome there is a Y-pattern, whereas a lambda pattern is present in SO overaction and an A pattern in IO paresis. To distinguish between a IO paresis and a SO overaction see head-tilt-test above. To make everything a bit more confusing, a Y pattern can also be present when there is an aberrant innervation of the lateral recti, in upgaze,^[42] or in the case of a bilateral inferior oblique overaction (see above).^[43]

Differential Diagnosis between DVD and Inferior Oblique Overaction

In inferior oblique overaction there is an increase of ipsilateral hypertropia in adduction to the contralateral side with a contralateral hypotropia, whereas in DVD, there is a hypertropia in adduction as well as in and abduction without a true contralateral hypotropia, when binocular fusion is interrupted. In order to evaluate this, the physician needs to check for a vertical deviation of the occluded eye, while the patient looks either side.^[4] Translucent occluders of Spielman are particularly helpful.^[44]

Vertical Strabismus Exam Findings by Etiology

Cause	Deviation and Motility	Pattern	Torsion	Deviation with head tilt	Forced Duction Testing	Other
Brown Syndrome	Elevation deficit and VS worst in adduction, occasional over-depression in adduction	None, Y, or V	None	No	Limited elevation in adduction
Inferior oblique palsy	Elevation deficit and VS worst in adduction	A	Intorsion	Worse with contra-lateral tilt		Associated superior oblique over-action
Superior oblique palsy	Depression deficit and VS worst in adduction	V pattern esotropia, worse if bilateral	Extorsion, typically >10 if bilateral	Worse with ipsilateral tilt, alternates if bilateral	Laxity of the SO	If bilateral, chin down position
Inferior oblique Overaction	Over-elevation in adduction. VS often limited to adduction	Y or V	Typically only objective Extorsion	No		Y pattern in primary; V pattern in secondary
Superior oblique Overaction	Over-depression in adduction. VS often limited to adduction	A or lambda pattern exotropia	Typically only objective Intorsion	No
Inferior rectus under-action	Depression deficit and VS worst in abduction		May have mild intorsion	Worse with contra-lateral tilt		Decreased force generation and saccadic velocity
Superior rectus under-action	Elevation deficit and VS worst in abduction		May have mild extorsion	Worse with ipsilateral tilt		Decreased force generation and saccadic velocity
Inferior rectus restriction	Elevation deficit and VS worst in abduction		May have mild extorsion		Limited elevation	Poor or absent Bell phenomenon
Superior rectus restriction	Depression deficit and VS worst in abduction		May have mild intorsion		Limited depression
Anti-elevation syndrome following inferior oblique anterior-ization	Elevation deficit and VS in abduction		Typically none		Limited elevation in abduction
Inferiorly displaced lateral rectus muscle	Over-depression and VS in abduction	V
Superiorly displaced lateral rectus muscle	Over-elevation and VS in abduction	A
Dissociated Vertical Deviation	Alternate cover testing shows an upward drift when the eye is covered, without a compensatory upward refixation of the fellow up		Extorsion

VS is Vertical Strabismus

Treatment Options

Monocular Elevation Deficit^[4]^[28]

If vertical deviation in primary position of gaze, attributable to a restriction of the IR on forced ductions: Inferior rectus recession. In the case of a large angle strabismus, a contralateral superior rectus recession may be indicated.

If superior rectus palsy: Superior transposition of half tendon lengths of medial and lateral recti or Knapp procedure. In the case of forced duction limitation, add an inferior rectus recession to the former.

Pseudo - Inferior Rectus Underaction (as in orbital floor fracture and muscle entrapment)^[4]^[2]

If due to restriction and minimal hypertropia in primary gaze: resection of the ipsilateral IR.
If a large hypertropia is present on primary gaze position: Ipsilateral IR resection + contralateral SR or IR recessions. An inverse Knapp procedure may be necessary.
In the case of orbital floor fracture with IR affection:
- Orbital floor repair, if indicated.
- If 8-15PD in primary position: Unilateral IR recession.
- If there is a large hypotropia in upgaze even in the case of a <8PD deviation in primary position: IR recession and an additional contralateral asymmetrical IR recession or contralateral SR recession may be indicated
- If >15PD in primary position: Ipsilateral IR recession plus contralateral SR recession.
- In pseudo-inferior rectus palsy with hypertropia in primary position: Ipsilateral muscle slack reduction through a plication + contralateral IR recession.

Superior Oblique Underaction

Unilateral:^[4]^[2]^[45]

If <10DP hypertropia in primary position, IO overaction more significant than SO underaction (deviation greater in upgaze): Ipsilateral graded inferior oblique anteriorization (weakening procedure)
If >15DP hypertropia in primary position (or deviation bigger in downgaze): Ipsilateral graded inferior oblique anteriorization + contralateral inferior rectus recession (yoke muscle).

Superior oblique tightening procedures - "tucks"- are indicated in congenital SO palsy with tendon laxity tested through forced duction or when there is minimal IO overaction with the vertical deviation being greatest in downgaze. This procedure may cause iatrogenic Brown syndrome.

If the deviation has become comitant due to superior and inferior rectus contractures, respective recessions should be performed

Bilateral:^[4]

In the case of a traumatic cause, it is advised to wait for 6 months and reevaluate for a potential recovery.

If main problem is extorsional diplopia (as in partially recovered post-traumatic paresis), with minimal hypertropia and V-pattern: Harada-Ito procedure.
If a big V-pattern, with >15DP esotropia in downgaze and >10º extorsion in primary position is present; reversing hypertropias in sidegaze: Bilateral Harada-Ito + bilateral medial rectus recessions with half-tendon width inferior transpositions or superior oblique tendon tuck + bilateral medial rectus recessions with half-tendon width inferior transpositions.
If masked bilateral involvement or asymmetric involvement is suspected: Bilateral IO graded anteriorization + contralateral IR recession or bilateral graded IO anteriorization + Harada-Ito procedure on the more affected side.

Inferior Oblique Underaction^[4]^[2]

If a vertical deviation in primary position, abnormal head posture or diplopia:
- If vertical deviation <10DP: Ipsilateral SO weakening (see superior oblique overaction)
- If vertical deviation of >10DP: Ipsilateral SO weakening + contralateral SR weakening.

Inferior Oblique Overaction ^[4]

If binocular fusion is compromised or for cosmetic reasons: A graded anteriorization of the IO is frequently sufficient. In this procedure it is important to keep the anterior IO fibers posterior to the IR insertion in order to avoid a hypercorrection and consequent hypodeviation.
- If bilateral, even if asymmetric: Bilateral IO weakening procedures (myectomy, recession, anteriorization) should be performed, except if amblyopia is present (surgery on the good eye is discouraged).
In the presence of a significant Y pattern in upgaze, even if there is no significant deviation in primary position or sidegaze: Bilateral IO weakening procedures

Superior Oblique Overaction^[4]^[46]^[47]

SO weakening procedures: SO expander, tenotomy, tenectomy or recession.

If the patient has binocular fusion, weakening the superior oblique may give rise to extorsional diplopia. In this particular case, horizontal muscle surgery or an expander may be more indicated, as suggested by Wright et al.^[4]

In the case of a coexisting DVD, particular care has to be taken since SO weakening procedures may worsen this entity.

Brown Syndrome^[4]

If inflammatory: systemic nonsteroidal anti-inflammatory agents, local steroid injection to the trochlea.
If congenital: There is an indication for surgery if there is a vertical deviation in primary position with an important face turn. SO lengthening procedures are indicated such as: SO expander, tenotomy, tenectomy. With tenotomy and tenectomy, care should be taken for overcorrections.

Duane Syndrome - the vertical component.^[4]

It may be addressed surgically with a Y-splitting procedure of the ipsilateral lateral rectus muscle.

Displaced Horizontal Recti^[4]^[2]

Relocate horizontal rectus muscle. Hereby, lateral recti are moved towards the open end of the pattern (up in V, down in A), while medial recti are transposed to the closed end of the pattern (down in V, up in A)

It is very important to correctly diagnose the cause of A and V patterns, because one may have the false impression of oblique muscle affection. If the A or V pattern is caused by a horizontal muscle displacement, it responds poorly to oblique muscle surgery.