Traumatic Motor Neuropathies (Third, Fourth, Sixth)

From EyeWiki


Disease Entity

Disease

Trauma to cranial nerve (CN) III (oculomotor nerve), CN IV (trochlear nerve) or CN VI (abducens nerve) will result in ocular motor dysfunction. These ocular motor cranial neuropathies can be isolated, meaning they affect only one nerve, or may impact more than one of the CN, meaning multiple cranial neuropathies[1]

Epidemiology[2][3][4]

The incidence of isolated CN IV palsy is the highest at 5.7 per 100,000 persons-year in comparison to CN III and CN VI palsy. CN VI palsy has the second-highest incidence rate at 4.7 per 100,000 person-years, and CN II palsy has the lowest incidence rate of all at 4 per 100,000 person-years. CN III palsy is more common above the age of 60 years, and is rare in the pediatric population. CN IV and CN VI nerve palsies appear to be more common in men.

Anatomy

Cranial Nerve III[5][6]

CN III originates in the ventral midbrain at the level of the superior colliculus. After exiting the midbrain medially to the cerebral peduncles, CN III splits into two branches in the superior orbital fissure: the superior division and the inferior division. The superior branch is responsible for the innervation of the superior rectus muscle and the levator palpebrae superioris, responsible for raising the upper eyelid. The inferior branch of CN III innervates the inferior oblique, the inferior rectus and the medial rectus. The CN III has two main layers: the inner somatic layer and the outer parasympathetic layer. The inner somatic layer supplies its respective extraocular muscles, while the outer parasympathetic layers supply the sphincter pupillae and ciliary muscles, responsible for the pupillary light reflex and accommodation. The parasympathetic innervation originates from the Edinger Westphal nucleus of the midbrain. In the setting of trauma, the outer parasympathetic layer is often the first to be damaged.

Cranial Nerve IV[7]

CN IV originates from the nucleus within the dorsal midbrain at the level of the inferior colliculus. The fascicles first travel posteriorly and inferiorly around the cerebral aqueduct to decussate upon their exit of the dorsal midbrain. These two nerve fascicles then wrap around the brainstem, each maintaining their contralateral sides and extending around the lateral brainstem to continue anteriorly. CN IV enters the cavernous sinus where a few sympathetic fibers contribute to the nerve fascicle. It then pierces into the cavernous sinus dura and follows CN III to enter the orbits at the superior orbital fissure. The superior orbital fissure is a common pathway for all three ocular motor CNs, and as such, is susceptible traumatic shearing forces. CN IV is responsible for innervating the superior oblique muscles, which allow the eye to abduct, depress, and internally rotate. CN IV has the longest course of any of the CNs, and is also the thinnest, also increasing its vulnerability in the setting of trauma.

Cranial Nerve VI[8]

CN IV nucleus is located at the level of the facial colliculus in the dorsal pons. Unlike the CN III and CN IV, CN VI is exclusively somatic, with no contributions from the autonomic nervous system and with no sensory function. CN VI contains two motorneurons that innervate the ipsilateral lateral rectus muscle and the contralateral medical rectus muscle . Approximately 40% of the nerve fascicles exit at the brainstem through the medial longitudinal fasciculus towards the contralateral medial rectus subnucleus. These fascicles then continue to innervate the medial rectus muscle which is responsible for bilateral coordination in lateral eye movement. The remainders of the axons from the abducens nucleus exit at the pontomedullary junction of the brainstem and travel superiorly and anteriorly in the subarachnoid space close to the base of the skull and the anterior inferior cerebellar artery. As such, in the setting of traumatic basal skull fractures, CN VI is at risk of damage. It then travels towards the upper clivus anchored to a fibrous sheath called Dorello’s Canal. CN VI is vulnerable to stretching due to this configuration. CN VI then follows the CN III and CN IV into the cavernous sinus before entering the orbit through the superior orbital fissure to its final destination, the lateral rectus muscle. CN VI has the second-longest course of any CN.

Pathophysiology

For detailed pathophysiology of each disease entity, please visit the previous EyeWiki articles on oculomotor, trochlear, and abducens nerve palsy.

Cranial Nerve III[9][10][11][12]

CN III has two main layers: the inner somatic layer and the outer parasympathetic layer. The inner somatic layer supplies its respective extraocular muscles, while the outer parasympathetic layers supply the sphincter pupillae and ciliary muscles, responsible for the pupillary light reflex and accommodation . Trauma as well as aneurysm, uncal herniation, or tumors will involve the superficial pupillomotor fibers . Non-compressive causes of CN III palsy, such as vascular lesions related to diabetes mellitus and hypertension, will less often affect the pupillary fibers (referred to as pupil-sparing CN III palsies).

Lesions of CN III can occur at any point along its trajectory. For more details on all types of lesions affecting CN III, please visit the oculomotor nerve palsy Eye Wiki previous article. In terms of trauma, CN III palsy occurs mainly at the level of the basilar, the interorbital, or the pupillomotor fibers. In the basilar region, both extradural or subdural hematomas secondary to head trauma can cause damage to the nerve. More specifically, these hematomas, with their mass effect, can cause intracranial hypertension and subsequently herniation, which results in a tentorial pressure cone, thus compressing the nerve as it passes over the tentorial edge. In the intraorbital region, trauma and tumors are the main causes of palsy. In the parasympathetic pupillomotor fibers region, “surgical lesions', which include trauma, uncal herniation, and aneurysm involve the pupil due to compression of the superficially located nerve fibers. Aberrant regeneration of CN III, also referred to as oculomotor synkinesis, occurs when there is damage to the endoneurial sheath. As such, this phenomenon may occur after an acute traumatic or compressive incident, but usually not in the presence of vascular etiologies such as diabetes mellitus as these etiologies do not impact the outer layer of the nerve . The incidence of this aberrant regeneration in traumatic CN III palsy is 15%.

Cranial Nerve IV[13][14][15][16][17]

CN IV palsies, when acquired in adulthood, are mostly due to trauma and microvascular disease. This is supported by the fact that CN IV is most vulnerable due to its long course and thin fragile configuration. Mild injuries to the head may cause traumatic CN IV palsy, in contrast with CN III and CN VI nerve palsies that require a stronger force of impact. In other words, most cases of traumatic CN IV palsies do not experience a profound loss of consciousness lasting over 30 minutes. CN IV palsies with traumatic etiologies often present bilaterally due to the decussation of the nerve fascicles upon their exit of the dorsal midbrain.

Cranial Nerve VI

Basal skull fractures can result in unilateral or bilateral CN VI palsy, as the basilar part of CN VI passes close to the base of the skull[18]. Changes in intracranial pressure (ICP) can also cause a CN VI palsy due to stretching of the nerve at the level of Dorello's canal[19] [20].

Lesion Location[21]

The general pathology related to traumatic CN palsies is not fully understood as there has been a poor correlation between trauma imaging results and specific cranial nerve palsies. For the ocular motor CNs, there are three main proposed locations of injury: at the level of the nuclei at the brainstem,[22] [23][24] the nerve’s exit of the brainstem, [25][26] and at the location in which nerves punctures the dura.

Risk Factors

The biggest risk factors for head injuries, which may cause ocular motor CN palsies, in older adults include polypharmacy, notably the use of antiarrhythmics, and environmental safety conditions, such as stair safety. [27] Risk factors for neonates include instrumental techniques of delivery, such as forceps delivery.[28] Children under the age of one are most at risk for severe head trauma.[29] High-contact sports are also more associated with traumatic head injuries.

Primary prevention

Various preventative strategies can be used to prevent head trauma in adults, such as implementing fall prevention strategies for older adults, wearing helmets when appropriate, and practicing vehicle safety, such as wearing a seat belt and never driving under the influence of drugs or alcohol.[30] In the pediatric population, additional safety measures can be implemented to keep the home safe, such as installing stair safety gates in the home.[31]

Diagnosis

History[32]

Assess the mechanism and severity of the trauma injury, including loss of consciousness, vomiting or nausea, amnesia, and Glasgow score (please refer to the Canadian Head CT rules[33]). Inquire about ophthalmic history and ocular symptoms: pain, blurry vision, diplopia, decreased visual field, swelling, tearing, and nystagmus. Characterize the diplopia in terms of onset and duration, monocular or binocular, vertical, horizontal or oblique displacement of the images.

Physical examination[32][34]

  • Ocular vitals signs: intraocular pressure (IOP), pupillary reflex and the presence of a relative afferent pupillary defect (RAPD), visual acuity  
  • Visual field defect
  • Extraocular motility
  • Strabismus testing: Cover and uncover test, prism alternating cover test and Maddox rod testing or double Maddox rod testing
    • To distinguish between restrictive strabismus and paretic strabismus: saccadic velocity testing (paretic eye will show floating saccades and increased latency)
  • Margin to reflex distance of the palperbral margins (ptosis assessment)
  • Hertel or Naugle exophthalmometer (proptosis, enophthalmos, hypoglobus)
  • Periorbital examination (edema, bone deformity, erythema, tenderness, wound entry or foreign body, eyelid laceration)
  • Complete ocular examination with funduscopy to assess for: wound entry or foreign body, chemosis, subconjunctival hemorrhage, corneal abrasion, iritis, hyphema, depth of the anterior chamber, traumatic cataract, optic disc edema.
  • Resistance to orbital retropulsion
  • Gonioscopy may be performed in case of intraocular foreign body (look for an entry wound)
  • If orbital fracture: forced-duction testing for possible extraocular muscle entrapment
  • If sixth nerve palsy: test corneal sensation (CN V function)


Emergent conditions that require intervention include, retrobulbar hemorrhage with compartment syndrome, ruptured globe, optic neuropathy (RAPD  and color vision), and retinal detachment

Signs

CN III palsy CN VI palsy CN VI palsy
Signs
  • Deviated primary gaze (exotropia and hypotropia) - "down and out"
  • Limited EOM in all directions (except abduction)
  • Ptosis
  • Pupillary involvement (mydriasis and poor pupillary reflex)
  • Limitation of inferior movement when patient looks nasally
  • Hypertropia of the involved eye in primary gaze (increase if they tilt their head toward the ipsilateral shoulder or asked to look in the direction of the intact eye)
  • Head tilt to the contralateral shoulder
  • Deficient abduction movement of the eye
  • Divergence insufficiency[35]
Other characteristics Traumatic injuries cause pupil-involving CN II palsy.


Traumatic injuries can result in aberrant regeneration of the CN3:

  • Eyelid-gaze dyskinesis : elevation of involved eyelid when the patient is ask to look downward (Pseudo-von Graefe sign) or nasally
  • Pupil-gaze dyskinesis: constriction of pupils when the patient is ask to look downward or nasally
  • Limitation of upward and downward gaze and with/without adduction of the involved eyes
  • Absent optokinetic response
  • Pupillary light-near dissociation


Note that a vascular/ischemic etiology does not typically cause pupil-involving CN III palsy and aberrant regeneration.

Diagnosis can be made via the Parks-Bielschowsky three-step test. Please refer to Cranial Nerve 4 Palsy


Bilateral CN VI palsy (common in trauma):[36][37] 

  • Crossed hypertropia
  • Double Maddox rod testing (extorsion of 10 degree and more for both eyes)
  • Large V-pattern esotropia (the eyes cross when looking downward) (25 prism diopters and more)
  • Bilateral fundus torsion
  • Head tilt (with chin depression)

Symptoms[32]

CN III palsy:

  • Binocular oblique diplopia
  • Ptosis


CN IV palsy:

  • Binocular vertical or oblique diplopia
  • Patient may report difficulty with reading or difficulty with going down stairs
  • Objects can seem tilted


CN VI palsy:

  • Binocular horizontal diplopia worse when looking to the ipsilateral side involved and in distance vision

Diagnostic procedures

The choice of head computed tomography (CT) should be based on Canadian Head CT rules.[38] Neuroimaging should be performed in case of involvement of more than one CN.[39] If a cervical spine injury is suspected, perform a cervical spine CT.[40][41] In case of a skull base fracture, perform a head CT.[42][43]

CN III palsy: Orbital CT (coronal views) to rule out orbital fracture. [44]

CN IV palsy: Brain CT should be obtained for initial evaluation.[45] Some studies report midbrain or cisternal concussion. [46]Brain magnetic resonance imaging (MRI) may be useful if the CT scan is normal. Some studies report lesions in the dorsal midbrain that were not visualized in the CT scans. [47]

*CN IV palsy is associated with low-intermediate head injury. In most of the case neuroimaging is unremarkable. [48]

CN VI palsy: Some studies recommend neuroimaging in all cases of traumatic CN VI palsy. Brain CT is usually the first line imaging modality. Brain MRI may be useful if the CT scan is normal.  Brain MRI is indicated in all children.[45] [49][50].

Other imaging modalities may be indicated to rule out associated injuries, such as orbital fracture (orbital CT and midface CT) and intraorbital foreign body (CT, MRI or B-scan).

Accompanying traumatic injuries

Orbital fracture[5][51]: Orbital fracture is most commonly associated with a CN III palsy, but can also be seen with CN IV or VI palsy. The fracture can compress or dissect the orbital portion of the CN. The orbital floor is the most common site, and the second most common being the medial wall .

Symptoms: binocular diplopia , pain on eye movement (e.g. pain in upward gaze if fracture of the orbital floor), oculo-cardiac reflex (nausea, vomiting, bradycardia) indicating muscle entrapment[52]

Signs: edema and tenderness, enophthalmos, subcutaneous emphysema, hypoesthesia in the territory of the involved nerve (e.g. infraorbital or supraorbital nerve), positive forced-duction test, increased IOP more than 4mm Hg  in the direction of limited movement

In the case of an orbital floor fracture and involvement of infraorbital nerve, patients can complain of hypoesthesia of the cheek and upper lip. If the supraorbital nerve is involved in the case of an orbital roof fracture, the patient can complain of hypoesthesia of the forehead and ptosis. In a zygomatic fracture, patients can report trismus, malar flattening and deformity.

*For patient with orbital fracture not complaining of any visual symptoms, ophthalmic evaluation could be done within 48h [32]

See  https://eyewiki.org/White-Eyed_Blow_Out_Fracture for more information

Intraorbital Foreign body[53][54]: Intraorbital foreign body can be associated with an ocular motor CN palsy by either compression or dissection of the nerve.

It may be asymptomatic or cause limitation of the eye movement, proptosis, diplopia, decrease vision, pain, palpable mass and other signs of ocular trauma.

*Always have a high index of suspicion of foreign body in all trauma (especially children)

*Avoid removing a foreign body  at the slit lamp if the depth of penetration is unknown

See https://eyewiki.aao.org/Orbital_Foreign_Body for more information.

An extraocular muscle rupture is uncommon and can be seen in penetrating trauma or blow-out fracture. The rupture can be surgically repaired, but if the eye does not regain its motility, nerve damage should be considered as the etiology of diplopia. [55][50][56]

Uncal herniation[57]: Uncal or transtentorial herniation can result in a CN III palsy by directly compressing the nerve  between the temporal lobe and the tentorium. It can cause contralateral or/and ipsilateral CN III palsy (in case of Kernohan’s notch). Patients with uncal herniation could present with cushing triad (bradycardia, abnormal breathing pattern, widened pulse pressure), altered mental status and other signs and symptoms of intracranial hypertension, contralateral homonymous hemianopia and absence of blinking reflex and contralateral hemiparesis (“false localizing signs”).

For an in-depth review of the uncal herniation, please visit: http://www.ncbi.nlm.nih.gov/books/NBK537108/

Cervical spine fracture[40][41]: Some traumatic injuries of the cervical spine can cause CN VI palsy by several mechanisms, i.e. whiplash injury,  hangman’s fracture and halo traction. Several case reports describe traumatic CN VI traction after a C2 distraction and a C1 ligamentous injury.

Patients can suffer from whiplash trauma and complain of tenderness to palpation, motor and sensory deficits (paraplegia, quadriplegia) , restriction of neck motility. According to the localization of the fracture, phrenic nerve palsy (above C5) and Horner syndrome (C8 to T1 injury) can also be observed. For an in-depth review of the cervical spine fracture, please visit: http://www.ncbi.nlm.nih.gov/books/NBK448129/

Basilar skull fracture can cause CN VI palsy. Signs of skull base fracture included racoon eyes sign, Battle’s sign, leak of CSF (rhinorrhea , otorrhea) and hemotympanum.[42][43] For an in-depth review of the basilar skull fracture, please visit: http://www.ncbi.nlm.nih.gov/books/NBK470175/

Differential diagnosis

Orbital floor fracture with muscle entrapment: ocular motor CN palsy can be distinguished from muscle entrapment in orbital fracture with the forced-duction test (negative for a palsy, positive for entrapment). Note that the force generation testing is abnormal in a ocular motor CN palsy.

Orbital edema and hemorrhage: Post-traumatic orbital edema and hemorrhage can cause limitation in movement of the extraocular muscles. However this should resolve within 7 to 10 days. Retrobulbar hemorrhage can also cause limited EOM.  

For detailed differential diagnosis of each disease entity, please visit the previous EyeWiki articles on oculomotor, trochlear, and abducens nerve palsy.

Management

General management

Although there are no clear guidelines for the management of traumatic ocular motor CN palsies according to current evidence, a few concepts remain constant regardless of which nerve is affected. First, any identified underlying cause should be addressed. In case of trauma, that means treating any intracranial condition such as a subdural hematoma or intracranial hypertension as a priority.[58]   Once intracranial lesion has been excluded, the mainstay of traumatic motor neuropathy management are observation and follow-up as for other etiology of ocular CN palsy.

Prognosis

Ocular motor CN palsy secondary to trauma and ischemia generally have good prognosis, as they tend to recover spontaneously over 6-9 months.[59][60]

Spontaneous resolution rates are variable among studies based on the definition of partial and complete resolution, as well as the small sample size. For example, Park UC et al defined the meaning of a complete recovery, partial recovery and persistence in a retrospective study on the natural history of acquired CN III, CN IV and CN VI palsy.[60] They reported partial recovery rate of nearly 100% at 6-months . In comparison, Park H et al reported a 47.5% spontaneous recovery of traumatic unilateral CN IV palsy.[61]

Regardless of these variations, certain characteristics at presentation seem to influence the prognosis of recovery. The angle of deviation at initial presentation is a significant prognostic factor for recovery, with the smallest angles of deviation having the best prognosis.[60] [61] Coello AF et al reported that a CN III palsy after a mild head trauma had a good chance to recover if no lesion was identified from the initial CT scan[62]. For traumatic unilateral CN IV palsy, Park H et al reported that the angle of deviation and fundus torsion are better predictive factors for spontaneous resolution than the factors related to trauma type, presence of intracranial lesion, loss of consciousness or Glasgow Coma Scale score[61].

Acute management

Monocular occlusion with a patch, Bengerter foil or frosted lens should be considered in all patients with symptomatic double vision.[63] Fresnel prisms can be a temporary option during the period of potential progressive resolution.[5] This option is especially useful when the angle of deviation is small. Correction of a less than 10 prism diopter (PD) is generally successful..[63]

Follow-up treatment with occlusion and prisms should continue at regular intervals until the ocular motor CN palsy resolves or stabilizes. Generally speaking maximal spontaneous improvement is typically achieved within 6-9 months after the traumatic event, regardless of the ocular motor CN involved. [5][63][64]

Chronic management

Once the deviation has become stable after adequate follow-up time, long-term management can be considered for residual symptomatic double vision. Prism and botulinum toxin injection can be offered as an alternative to surgery . [5][63][64]

Permanent prism can be incorporated into patient’s spectacle. As for acute management, the angle of deviation can be a limitation for a successful management with this option.[5] In case of residual esotropia, permanent prism can be combined with botulinum toxin injection.[63]

Botulinum toxin injection is a treatment option to manage diplopia i.[63] By blocking the release of acetylcholine at the motor endplates of neuromuscular junctions, Botulinum toxin prevents muscle contraction, thus causing a temporary paralysis of the extraocular muscle injected. This allows the opposing muscles to align the eye by taking on a greater force movement.[65][64] This intervention is rarely curative, but it alleviates diplopia and compensatory anomalous head posture.[64] In the case of CN VI palsy, the injection is made into the ipsilateral medial rectus muscle under topical anesthesia and possibly with electromyographic guidance.[65] [66]Preventing contracture of the medial rectus in the affected eye might be another advantage of botulinum toxin injection [64][66]. It can also be used to diminish the angle of deviation and ease correction with permanent prisms.[5] A Cochrane review rated the effectiveness of botulinum toxin injection as low[67] Injection of botulinum toxin into the inferior oblique muscle to treat an acute traumatic CN IV palsy and into the lateral rectus muscle to treat an acute traumatic CN III palsy have also been described[68][69]. Although the results from the clinical trials of small samples have shown potential benefits of these procedures, their clinical use seems to be limited due to their possible complications.[64] [68][69] Once the injection is done, the effect will gradually increase until it reaches its maximum 1–2 weeks after the procedure. The effect is temporary and will dissipate within 3 months.[5] The injections will therefore have to be repeated every 3-4 months indefinitely or until the next step of management (i.e. surgery). [64]

Strabismus surgery aims to relieve diplopia by restoring binocularity and alleviating normal head positioning if present. CN III palsy is difficult to treat surgically as it generally involves several extraocular muscles. Several techniques have been described. The presence of ptosis can also be addressed surgically at this stage of management.[70] Surgery is frequently required for traumatic CN IV palsy.[5] The surgical indications include deviation greater than 10 PD and unsuccessful prism treatment.[63] Different surgical options are possible: strengthening of the superior oblique muscle (tuck procedure), myectomy or recession of ipsilateral inferior oblique muscle and/or recession of the contralateral inferior rectus muscle. [5][59] The magnitude of the deviation will guide the choice of procedure. Excyclotorsion might also need to be corrected with specific procedures, mostly with bilateral CN IVpalsy.[5] For CN VI palsy, surgical intervention also depends on the severity of the palsy. In case of partial paralysis, a lateral rectus resection and medial rectus recession in one eye or bilateral medial rectus recessions can be considered. A combination of weakening of the ipsilateral medial rectus and transposition of the superior and inferior recti above and below the affected lateral rectus muscle can be used to treat a complete CN IV palsy.[5]

For more information on strabismus surgery, please refer to these EyeWiki articles:

https://eyewiki.org/Strabismus_Surgery,_Horizontal

https://eyewiki.org/Strabismus_Surgery,_Vertical

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