Introduction

Duane retraction syndrome (DRS) is a congenital mis-innervation syndrome affecting the ocular motility characterised by agenesis of the abducent nerve with the inferior division of the oculomotor nerve splitting to innervate both the lateral and medial rectus muscles [1,2,3]. The co-contraction of both medial and lateral rectus muscles can result in narrowing of the palpebral fissure and retraction of the globe on attempted adduction [4, 5], which is a major hallmark in the diagnosis of DRS. In addition, all types of Duane syndrome are associated with limitation of either adduction, or abduction or both. The limitation of movement is seen clinically in both ductions and versions.

For the past few years, the authors noted that some patients present with patterns of strabismus that share some of the clinical features of Duane syndrome, but do not fulfil the complete criteria to confirm the diagnosis. The majority of these patients presented with small exotropia—or less commonly esotropia—of one eye in the primary position with a compensatory face turn to the contralateral side in exotropic patients and to the ipsilateral side in esotropic patients. These patients showed horizontal gaze incomitance with the deviation increasing on gazing in the direction of the face turn, which explains why the patient adopts this face turn. However, contrary to what is seen in Duane retraction syndrome, these patients either had no retraction of the globe on attempted adduction or no obvious limitation of adduction or abduction on ductions and versions testing. The aim of this study is to report these incomplete patterns that do not fulfil the full clinical pattern of Duane syndrome, and to describe both their clinical findings and the results of their surgical management.

Methods

The study protocol was approved by the Research Ethics committee of L V Prasad Eye Institute and Cairo University. The study and data collection conformed to all local laws and were compliant with the principles of the Declaration of Helsinki. A retrospective study was performed on all patients with a diagnosis of exotropia or esotropia associated with a face turn.

The study population consisted of patients who showed non-comitant exotropia or esotropia in the horizontal gazes and had a constant face turn to correct for this incomitance with an onset in the first year of life. Patients were included if they showed either globe retraction on adduction or limitation of adduction or abduction on ductions but not both retraction and limitation, along with ipsilaterally tight horizontal muscles on forced duction test (FDT). Patients who had prior eye muscle/orbital surgery or trauma or any acquired or coexisting neurological causes were excluded from the study. Patients were divided into two main groups according to their clinical features; those with limitation of eye movement but with no globe retraction on adduction (sine retraction), and those with globe retraction on adduction but no more than −0.50 limitation of eye movement on ductions testing (sine limitation).

All patients had a detailed sensorimotor examination during the initial evaluation and at each follow-up. This included measurement of uncorrected and best-corrected visual acuity, cycloplegic refraction and evaluation of fundus for torsion if present using indirect ophthalmoscopy. The ductions and the versions of all patients were analysed. Underaction was graded on a subjective scale of 0 to −4 with 0 indicating no underaction and −4 indicating failure of the eye to cross the horizontal midline. A trace or −0.50 underaction was defined as no limitation of ocular movement on duction testing, but with an increase in the angle of deviation in this gaze by 5 prism dioptres (PD) more than the primary position. Overaction was graded similarly on a scale of 0 to +4 [6].

Globe retraction was evaluated by a subjective scale as follows: with the involved eye in the maximum adducted position, a scale is used at the centre of the palpebral fissure width to measure the palpebral aperture height and compared with that of the fellow eye in abduction. Grade 0—no narrowing, grade 1—25%, grade 2—25–50%, grade 3—50–75% and grade 4—>75% [7]. Upshoots were graded on a subjective scale similar to the one used for inferior oblique overaction from 0 to +4; with +1 indicating minimal discrepancy between both eyes and +4 indicating marked discrepancy between both eyes during versions. All patients were evaluated very carefully for the presence of globe retraction and or adduction/abduction limitation. The description of the same was noted in the file of each patient. All had nine gaze photographs, which was analysed additionally.

The angles of horizontal and vertical misalignment were measured by the prism and alternate cover tests for both distance and near. In addition, the angles of horizontal and vertical misalignment were measured in side gazes (at distance, head position at 25°) for lateral incomitance, in up and down gazes to look for any pattern as well as in right and left head tilts. Any abnormal head posture, if present was noted.

In those who had surgical intervention, the details of surgery and its outcomes were recorded. Surgery was mainly recession of the tight muscle as determined on FDT. Surgery was done through either limbal or fornix approach. A small conjunctival recession 1–2 mm was added at the end of surgery in cases with limbal approach. Moreover, those with clinically significant upshoots and/or downshoots on adduction, underwent Y-splitting of the lateral rectus. Data obtained after surgery was compared with the baseline measurements using the paired t test for continuous variables and Wilcoxon signed rank test for ranks and scores.

Results

Twenty-one patients who fulfilled the inclusion criteria were identified, 13 males and 8 females. The mean age of the included patients was 8.0 ± 4.6 (range: 4–18) years and the onset misalignment of eyes was noted within the first year of life, with no history of trauma or neurological deficit. The left eye was affected in 15 patients (71%), while the right eye was affected in 6 patients. Most common presentation was exotropia seen in eighteen patients (86%). Thirteen patients were included in sine retraction group, while 8 patients in sine limitation group. Five patients underwent detailed MRI brain and orbit out of which one patient in the sine retraction group had absent ipsilateral sixth nerve while others were normal. For those who had surgery, the mean follow-up period was 37.3 ± 13.0 months (range: 3–48 months).

Sine retraction group

In the sine retraction group, three patients presented with esotropia, while ten patients had exotropia in the primary position. The left eye was affected in nine cases, two in esotropia and seven in exotropia group (Table 1).

Table 1 Preoperative and postoperative characteristics of patients with Duane sine retraction.
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Primary deviation in three patients with esotropia ranged from 8 to 20 PD, which increased on ipsilateral gaze (range: 30–45 PD) and disappeared on contralateral gaze similar to what is seen in Type I Duane syndrome but with no retraction of the globe on adduction (Fig. 1). Two patients showed small esotropia of 8 PD which was out of proportion to the severe abduction limitation of −4 in the affected eye. All patients adopted an ipsilateral face turn that ranged from 5 to 20°. Two patients showed +1 upshoot on adduction. All three patients had an ipsilateral tight medial rectus muscle on FDT and underwent 4 mm ipsilateral medial rectus recession to correct the esotropia and face turn. Following surgery, two patients were orthotropic in primary position, the angle of deviation on ipsilateral gaze ranged from 25 to 40 PD with no face turn while one patient showed a residual esotropia of 5 PD with small residual face turn of 5°. No change in upshoot was noted post-operatively.

Fig. 1: Sine retraction: Image showing a patient with exotropia of 4 PD in primary gaze, −3 limitation of abduction and −1 limitation of adduction in left eye suggesting a type 3 DRS.
figure 1

He had minimal left face turn and right head tilt. Please note the absence of retraction or narrowing of palpebral fissure height on adduction in the left eye. MRI brain revealed absence of left abducens nerve while the right abducens nerve was well developed (yellow arrows) (color figure online).

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All ten patients presenting with exotropia in the primary position (range: 4–25 PD) showed an increase in deviation in contralateral gaze (range: 14–40 PD) and disappeared on ipsilateral gaze as seen in exotropic Duane syndrome but with no retraction of the globe on adduction, adopting a contralateral face turn that ranged from 5 to 15°. All patients showed some limitation of adduction of the affected eye (range: −0.5 to −3), but with vast majority of them (six patients, 60%) showing only −0.5 limitation of adduction. Four out of these six patients had significant up or downshoot on adduction while two cases had mild abduction limitation of −0.5, which helped to diagnose them as DRS in spite of no retraction on adduction and minimal limitation of motility. Four patients showed some limitation of abduction of the affected eye (range: −0.5 to −3). A total of eight out of ten patients showed upshoots and/or downshoots on adduction while five showed pattern strabismus (V pattern in two patients, X pattern in two patients and A pattern in one patient). Surgery was offered to all ten patients, but only seven consented for the same and underwent a 5–8 mm ipsilateral lateral rectus (LR) recession that was found to be tight on FDT. The lateral rectus recession was combined with a 15 mm Y-splitting in two patients with significant upshoot and downshoot. Following surgery, six patients were orthotropic in primary position with no face turn. The angle of deviation on contralateral gaze ranged from 5 to 12 PD. One patient showed a residual exophoria of 5 PD, but no corrective face turn. Following the Y split of LR, upshoot (preoperative = +2) and downshoot (preoperative = +3) resolved completely suggestive of mechanical overshoots.

Sine limitation group

In the sine limitation group (n = 8 patients), the left eye was affected in six patients. All patients presented with exotropia in the primary position (range: 5–20 PD), that increased on contralateral gaze (range: 10–30 PD) and disappeared on ipsilateral gaze as seen in exotropic Duane syndrome, adopting a contralateral face turn that ranged from 5 to 15° (Table 2). All eight patients showed some retraction of the globe on adduction, that was however less obvious than that usually seen in exotropic Duane syndrome (range: 0.5–2) None of the patients showed limitation of adduction of the affected eye on duction testing, but all patients showed an increase in exotropia on contralateral gaze, suggestive of −0.5 limitation of adduction (Fig. 2a, b). In addition, one patient showed trace limitation of abduction of the affected eye. Seven of the eight patients showed upshoots and/or downshoots on adduction and four patients showed pattern strabismus (V pattern in three patients and X pattern in one patient), which along with retraction helped in making a diagnosis of DRS in spite of no obvious limitation of motility. Only seven patients consented for surgery and underwent 5 mm ipsilateral lateral rectus recession that was found to be tight on FDT, to correct the exotropia and face turn. The lateral rectus recession was combined with a 15 mm Y-splitting in one patient with significant upshoot (+2) as well as downshoot (+1). Following surgery, six patients were orthotropic in the primary position with the angle on contralateral gaze ranging from 5 to 12 PD. None of them showed face turn. The remaining patient showed a residual exophoria of 4 PD, but no corrective face turn. Retraction had resolved in most cases (five patients, including the one who underwent LR Y split), while three cases had residual 0.5 grade retraction. Overshoots had resolved in six cases while two had minimal upshoot of +0.5 grade.

Table 2 Preoperative and postoperative characteristics of patients with Duane sine limitation.
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Fig. 2
figure 2

a Sine retraction and sine limitation: Pre operative images of the patient showing left face turn of 15° with small exotropia in the primary position that increases on left gaze. There is no retraction of the globe and narrowing of the palpebral fissure of the left eye on attempted adduction, no clinically obvious limitation of adduction of the left eye (preoperative). b Image showing no face turn and orthotropia in the primary position. There is no retraction of the globe and narrowing of the palpebral fissure of the left eye on attempted adduction, no clinically obvious limitation of adduction of the left eye (postoperative: Lateral rectus muscle recession in the left eye).

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Discussion

Duane retraction syndrome was first described more than a century ago by Stilling (1887), Türk (1899) and Alexander Duane (1905) [8]. In the European literature, it is often referred to as the Stilling–Turk–Duane syndrome. The diagnostic clinical features of DRS are narrowing of the palpebral fissure and retraction of the globe on attempted adduction that is associated with a complete or partial limitation of ocular motility. The condition is sometimes associated with upshoots and/or downshoots on adduction. Patients frequently adopt an abnormal head posture to maintain fusion [8].

Although the reported incidence of esotropic Duane is much higher than the exotropic type, most of our cases presented with exotropia (86%) with or without limited adduction, similar to what is seen in type 2 Duane syndrome. One possible reason for the high incidence of exotropic cases in our study is that these patients would probably be underdiagnosed as Duane syndrome and rather as exotropia with horizontal incomitance. The left eye was more commonly affected in our study, similar to that of Duane syndrome. All patients had a history of strabismus since birth.

Aberrant innervation to lateral rectus from third nerve causes co-contraction of both the medial rectus and the lateral rectus muscle on attempted adduction resulting in narrowing of the palpebral fissure and retraction of the globe on attempted adduction. This abnormal innervation was first described by Scott et al and was proved later by electromyographic studies [9, 10]. Both the retraction of the globe and the limitation of ocular motility are considered diagnostic features of DRS that differentiate it from other patterns of strabismus and their absence makes the diagnosis of DRS questionable. In this study, we are reporting patients who presented with some features of DRS, but did not fulfil the complete diagnostic criteria. These patients either had no retraction of the globe on attempted adduction or no limitation of the ocular motility on ductions and versions. Nevertheless, these patients presented with an abnormal face turn and a horizontal gaze incomitance with the angle of misalignment increasing in the ipsilateral gaze of face turn and decreasing on the contralateral gaze of face turn, similar to what is seen in Duane syndrome. Most often the alignment in primary position was found to be out of proportion to the motility limitation. Moreover, the face turn and misalignment in primary position either disappeared or improved following surgery on the affected eye confirming the diagnosis.

Most of the patients in the present study showed an over-elevation and/or over-depression of the globe on attempted adduction. All patients showed unilateral tightness of the affected muscle on FDT, which may slip under or over the globe on attempted adduction and result in abrupt upshoot and/or downshoot of the affected globe, mimicking the upshoots and downshoots seen in Duane syndrome. Another theory that might explain the abrupt upshoot or downshoot is aberrant innervation of the vertical and/or the oblique muscles with co-contraction of the vertical and medial rectus muscle [7]. Overshoots helped in making a diagnosis of DRS in cases of doubtful clinical features in this study.

O’Malley and Helveston reported that some patients with Duane syndrome might have other additional abnormalities of the eye such as coloboma, limbal dermoid, or systemic associations like sensorineural deafness or haemangioma. They suggested the use of the term Duane’s retraction syndrome—plus in these patients [11]. In this study we propose using a collective term of Duane syndrome—minus, due to the lack of one of the cardinal diagnostic features and includes the following two subsets: (1) Duane sine retraction: lack of retraction of globe and narrowing of the palpebral fissure on attempted adduction and (2) Duane sine limitation: lack of clinically obvious limitation of the ocular motility on examination. While we agree that many might argue whether these patients have Duane syndrome, we only aim to report and to link these particular patterns to the nearest ocular motility disorder, rather than to prove that these patients have the exact pathogenesis of Duane syndrome. Previously, some studies have reported a subclinical or “forme fruste” variant of Duane syndrome in family members of affected patients who showed extraocular muscle paresis (other than lateral rectus paresis) or minimal retraction during horizontal ductions [12]. Sporadic cases without any family history similar to Duane sine retraction in our study have also been reported [13]. However, Duane sine limitation has not yet been reported.

The absence of globe retraction and the subtle limitation of ocular motility might be due to the young age of our patients and the possible incomplete appearance of the full clinical picture of Duane syndrome. Globe retraction may possibly become more evident with time as the lateral rectus becomes progressively fibrous [13]. Another explanation could be possible weak paradoxical innervation of horizontal muscles in these patients. We suggest that the co-innervation of medial and lateral rectus may not be strong enough to produce clinically obvious retraction resulting in sine retraction. While in the sine limitation group, the innervation of lateral rectus from abducens nerve may remain intact resulting in good abduction, along with some amount of mis-innervation from medial rectus, leading to co-contraction and retraction of the globe with mild adduction limitation. As both genetic and environmental factors are likely to play a role in the development of Duane syndrome, the suggested weak paradoxical innervation of horizontal muscles may be attributed to variable expressivity of abnormal genes.

A major limitation of our study is the absence of confirmatory evidence of Duane syndrome by electromyography. Although, agenesis of abducens nerve was seen on MRI brain in one patient which provides some anecdotal evidence supporting the diagnosis of DRS showing similar etio-pathogenesis. While we wished to perform electromyography in our patients to confirm the diagnosis and to test the presence of paradoxical innervation, the relatively young age and financial constraints of our patients made this difficult.

In conclusion, we suggest that some patients may present with ocular motility pattern similar to what is seen in Duane syndrome but lack the complete picture to confirm its diagnosis. Such patients might go unnoticed or misdiagnosed as exotropia or esotropia with horizontal gaze incomitance, such as due to nerve palsies. The congenital nature of the condition, presence of a face turn, overshoots on adduction, ipsilateral tightness of the affected muscle and presence of retraction on adduction in case of near normal motility should make the clinician consider Duane minus syndrome with either sine retraction or sine limitation. The patients in our study responded well to lines of management similar to those of Duane syndrome.

Summary

What was known before

  • Duane syndrome and its features are well known to ophthalmologists.

What this study adds

  • Duane syndrome minus patients do not have all the features of typical Duane syndrome subjects, but they respond to the surgical techniques used in Duane syndrome.

  • This should not be confused with paralytic strabismus or comitant strabismus.