Duane retraction syndrome (DRS) is the most common congenital ocular motility disorder caused by abnormal ocular innervation.1,2 Abnormalities of eye movements in the horizontal direction and horizontal strabismus are the most common clinical manifestations, while vertical strabismus which usually occurs in Huber type III patients is less commonly observed.3,4 Researches in ocular electromyography (EMG), neuropathology, neuroimaging and more recently, in molecular genetics of patients with DRS suggest that hypoplasia of the abducence nerve and extra branch of the inferior division of the third cranial nerve (CN3) to the lateral rectus are the major causes of this syndrome.5–7 Studies using ocular EMG in DRS patients have also found additional abnormalities, such as paradoxical innervation between horizontal rectus muscles and vertical rectus muscles,8 and dual innervation of medial rectus muscle.9 Magnetic resonance imaging (MRI) studies have shown hypoplasia of vertical rectus muscle and oblique muscles in some patients with DRS.10 The various abnormalities mentioned above reflect the heterogeneity of the clinical manifestation of the disease.
The purpose of the study was to investigate the effects of superior rectus (SR) recession for vertical deviation and A pattern in 5 patients with Duane syndrome type III. Ocular motility examination and MRI of the extraocular muscles and the corresponding cranial nerves were analyzed together in order to find a rational, customized, and individualized treatment based on the pathogenesis of the disease.
Five patients of DRS Type III with vertical strabismus were included in this case series study. The diagnosis was based on Huber's classification and clinical features. Signed informed consents were acquired before MRI and surgery. All procedures were in accordance with the Declaration of Helsinki.
Ophthalmic examination included measurement of the ocular deviation, binocular sensory function for fusion (synoptophore analysis) and stereopsis (TNO test) before and after surgery. During surgery, ocular motility was examined with particular attention to the relation between corrected ocular motility and recession of the superior rectus and lateral rectus.
MRI was performed before surgery with a General Electric 1.5-T Twinspeed scanner. Imaging of the ocular motor nerves in the brainstem was performed in 0.8-mm thickness image planes using the 3D-fast imaging employing steady-state acquisition (FIESTA) sequence (TR, 4.8 ms; TE, 1.4 ms; FOV, 18 × 18 cm; matrix, 256 × 256; NEX, 4). Nerves innervating extraocular muscles (EOMs), EOMs and their associated connective tissues were imaged with a T1-weighted fast spin-echo (FSE) in triplanar scans by dual-phased coils (TR, 440 ms; TE, 12 ms; slice thickness, 2 mm; interslice gap, 0.3 mm; FOV, 10 × 10 cm; matrix, 224 × 256; ETL, 2; NEX, 2).
All surgery was performed under subconjunctival anesthesia. Ocular alignment and ocular motility was observed during the surgery. Superior rectus muscle was recessed to correct vertical strabismus and A pattern. Lateral rectus muscle was recessed for upshoot and associated exotropia. Restriction of the muscles was decided by forced duction.
The clinical and imaging characteristics are summarized in Table 1. Systemic and neurologic examinations were negative in all cases. All subjects had unilateral variable limitation of both abduction and adduction, with palpebral fissure narrowing and globe retraction in adduction, and retraction of the eyeball was aggravated with down gazing in adduction. Three cases had A pattern strabismus. Three cases had hypertropia. MRI studies revealed hypoplasia or absence of the affected abducens nerve in the brainstem in all patients (Figures 1A and 2A). Case 1 and 5 had lager oculomotor foramen on the affected side (Figures 1B and 3A). Case 2 and 3 had hypoplasia of the superior rectus and inferior rectus (Figure 2 D and E). There was presumably a branch of CN3 innervating the LR in Case 1 (Figure 1 C and D), two branches of CN3 sent into medial rectus were revealed in Case 2 (Figure 2 B and C), contiguous coronal MRI of the orbit showed inferior division of the oculomotor sending out a branch coursing along the superior rectus muscle and the optic nerve in Case 5 (Figure 3 B and C).
Adduction of the affected eye had improved and the innervational upshoot on adduction was eliminated in all patients after recession of the lateral rectus muscle 8-12 mm. Recession of the superior rectus muscle reduced vertical deviation in the primary position and corrected A-pattern in 3 patients (cases 1, 3 and 5). Case 3 had bilateral overdepression on adduction and A-pattern exotropia with 40Δ exdeviation in upgaze and 60Δ exdeviation in downgaze. During the operation, the most striking motility phenomenon in this patient was that recession of the left lateral rectus muscle caused reduced depression and 10° hypertropia of the affected eye. Therefore, left superior rectus recession and suspension of 7 mm was performed to correct the deviation. Case 4 did not have any horizontal deviation in the primary position preoperatively. She received 10-mm recession of a slightly tight left superior rectus combined with 8-mm tight left lateral rectus recession. The patient developed 10Δ esotropia postoperatively but she did not complain of diplopia.
All patients underwent the operation under local anaesthsthesia with 2% lidocaine, which allows examination of the position and movement of the eyes during operation. During the operation, after the affected eye received lateral rectus recession and suspension, adduction improved obviously and upshoot on adducted position disappeared. However, there was residual vertical deviation, showing that co-contraction of the lateral and the medial rectus was the major mechanism responsible for the limitation of adduction and upshoot on attempted adduction.11 All five patients turned their faces away from the affected side to compensate for the limited adduction and upshoot instead of the limited abduction preoperatively. However, limitation of abduction was worse after operation, while the compensated head position disappeared or turned to the affected side to compensate for the limited abduction.
Significant A pattern was observed in 3 patients. Ocular motility examination revealed increased retraction on adducted depression and limitation of depression on abduction of the affected eye in all 3 patients. It seemed that the A pattern was caused by overreaction of the bilateral superior oblique muscles. However, the preoperative MRI had shown hypoplasia of the superior and inferior rectus of the affected eye in two cases. After recession of the superior rectus, both over depression on adduction and A pattern improved. Patient 3 had exotropia in the primary position preoperatively. Contiguous quasicoronal MRI revealed two branches of CN3 to the medial rectus and hypoplasia of the superior rectus. Intraoperative examination showed that recession of the lateral rectus of the affected eye resulted in 10° hypertropia and limitation in downgaze. Superior rectus recession was performed according to the above findings. Therefore the structural abnormalities of the vertical muscles or abnormal innervations between the horizontal and the vertical rectus muscles may explain, at least partially, the cause of A pattern and vertical strabismus in DRS type III.
As the most common congenital restrictive ophthalmoplegia, pathogenetic studies of DRS indicate that innervational and mechanical factors are responsible for the restriction and abnormality of ocular movement.12 All 5 cases in this study had dysplasia of abducens nerve as revealed by MRI. Especially orbital MRI revealed lager oculomotor foramen in two patients. The affected muscles, the extent of abnormality and the abnormal innervation were different in different cases. Given the various abnormalities that may be the cause of DRS, it is very important to design the surgery individually. Local anaesthesia leaves patients conscious during the surgery, which gives doctors an opportunity to choose appropriate surgical procedures and amount of operation.
Patients with DRS often have compensated head position to allow binocular fusion. Case 2 in this report had inconsistent objective and subjective strabismus angle preoperatively. He had 30Δ exdeviation with 40Δ hyperdeviation in the primary position, but he fused on the synoptophore with an angle of +3R/L4°. After operation, while a residual small-angle hypertropia was observed, paradoxical double vision occurred. This phenomenon seems not to be caused simply by anomalous retinal correspondence. The effect of abnormal innervation on binocular vision remains a subject for further study.
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