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Show Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Magnetic Resonance Imaging Findings in Patients With Duane Retraction Syndrome Yatu Guo, MD, PhD, Quan Zhang, MD, PhD, Tingting Zhang, MD, Lingzhi Guo, MS, Shichang Liu, MD, PhD, Kanxing Zhao, MD, PhD, Wei Zhang, MD, PhD Background: Duane retraction syndrome (DRS) is known to relate to the absence of the abducens nucleus, with abnormal innervation of the lateral rectus (LR) muscle by branchesof the oculomotor nerve (CN III). The purposes of this study were to investigate the morphological characteristics of the oculomotor nerve (CN III), the abducens nerve (CN VI), and the extraocular muscles in patients with clinically diagnosed Duane retraction syndrome (DRS) using MRI. In addition, we assessed the association between ocular motility, horizontal rectus muscle volumes, and CN III/VI in patients with Duane retraction syndrome (DRS). Methods: The study comprised 20 orthotropic control subjects (40 eyes) and 42 patients with Duane syndrome (48 eyes), including 20 patients with DRS Type I (24 eyes), 5 patients with DRS Type II (6 eyes), and 17 patients with DRS Type III (18 eyes). Three-dimensional (3D) T1/2 images of the brainstem and orbit were obtained to visualize the cranial nerves, especially the abducens (VI) and oculomotor (III) nerves, as well as extraocular muscles. Tianjin Eye Hospital (YGD, KZD, WZD), Tianjin, China; Nankai University Affiliated Eye Hospital (YGD, KZD, WZD), Tianjin, China; Tianjin Key Lab of Ophthalmology and Visual Science (YGD, KZD, WZD), Tianjin, China; Tianjin Medical University (LG), Tianjin, China; Department of Radiology (QZD), Characteristic Medical Center of Chinese People’s Armed Police Force, Tianjin, China; Shandong Lunan Eye Hospital (TZ), Shandong Medical College Affiliated Eye Hospital, Linyi, China; and Department of Radiology (SLD), Tianjin Medical University Cancer Institute and Hospital, Tianjin, China. Supported by the National Natural Science Foundation of China (No. 81300791), the Natural Science Foundation of Tianjin (No. 18JCYBJC26500), the Tianjin Science and Technology support key Project (No. 19YFZCSY00990), the Tianjin Health Research Project (Nos. TJWJ2021MS042 and TJWJ2022XK037), Key Project of Tianjin Eye Hospital (No. YKZD2004), the third Tianjin Talent Development Program and the High-level Talents Program in TJHS Tianjin Key Medical Specialty Construction Project, and Tianjin Key Medical Discipline Construction Project (No. TJYXZDXK-016A). The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www. jneuro-ophthalmology.com). Y. Guo, Q. Zhang, and T. Zhang contributed equally to the work. Address correspondence to Wei Zhang, MD, PhD, Heping District, Gansu Road 4, Tianjin, China; E-mail: weizhang3067@163.com This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 Results: Based on the clinical classification, among 42 patients, MRI showed that the abducens nerves (CN VI) on the affected side were absent in 24 of 24 eyes (100%; 20 patients) with Type I DRS and in 16 of 18 eyes (88%; 16 patients) with Type III DRS. However, CN VI was observed in 6 of 6 eyes (100%; 5 patients) with Type II DRS and in 2 of 18 eyes (11%) with Type III DRS. CN III was observed in all patients. The oculomotor nerves on the affected side were thicker than those on the nonaffected contralateral side in DRS Type I (P , 0.05) and Type III (P , 0.05), but not in DRS Type II. Smaller LR and larger MR volumes were shown in the affected eye than that in the nonaffected eye in DRS Types I and III. Based on the presence or absence of CN VI, there was a tendency for thicker oculomotor nerves in the affected eye than in the nonaffected eye in the absence groups (P , 0.05). However, no significant difference was found in the present group. In the CN VI absence groups, similar results were found in the affected eyes than in the nonaffected eyes as in DRS Types I and III. In addition, the presence of CN VI was correlated with better abduction (P = 0.008). The LR and MR volumes have positive correlations with the oculomotor nerve diameter in the affected eye. However, there was no correlation between the range of adduction/abduction and the LR/MR ratio in patients with or without an abducens nerve. Conclusions: Different types of DRS have different characteristic appearances of CN VI and CN III on MRI. Horizontal rectus muscles have morphological changes to adapt to dysinnervation of CN VI and aberrant innervation of CN III. Thus, these neuroimaging findings may provide a new diagnostic criterion for the classification of DRS, improving the comprehension of the physiopathogenics of this disease. Journal of Neuro-Ophthalmology 2024;44:101–106 doi: 10.1097/WNO.0000000000001909 © 2023 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the North American Neuro-Opthalmology Society. D uane retraction syndrome (DRS) is a congenital oculomotor disorder characterized by limited horizontal eye movement with palpebral fissure narrowing and globe retraction on attempted adduction.1 Huber divided DRS into 3 types: abduction limitation in Type I, adduction limitation in Type II, and limited abduction and adduction in Type III.1 With a greater understanding of this form of strabismus, it is now considered as a congenital cranial dysinnervation disorder (CCDD) with underlying pathophysiology of abducens nerve agenesis and various degrees of aberrant innervation of the lateral rectus (LR) muscle by the ipsilateral oculomotor nerve.2,3 101 Original Contribution The presence of CN VI depended on the type of DRS that has been reported.2,4 However, the etiology of different types of DRS remains controversial.2–4 In addition, the anormogenesis of CN III and CN VI and its relationship with extraocular muscle (EOM) size and ocular motility need to be further investigated. This study was performed to characterize the morphology of CN III/VI and their association with ocular motility and EOM volumes using MRI. METHODS We obtained approval from the Ethics Review Committee of Tianjin Eye Hospital and conformed to Declaration of Helsinki. All participants provided written informed consent. Twenty normal subjects and 42 patients diagnosed with DRS who visited Tianjin Eye Hospital from April 2015 to August 2021 were recruited. All patients received a complete ophthalmologic examination. Clinical characteristics of subjects are summarized in Supplemental Digital Content 1 (see Tables S1–3, http://links.lww.com/WNO/ A714, http://links.lww.com/WNO/A715, http://links.lww. com/WNO/A716). Designation in different grades of abduction/adduction deficit is as follows: no deficit (0): full rotation; deficit (21): from the midline to 75% of full rotation; deficit (22): from midline to 50% of full rotation; deficit (23): from midline to 25% of full rotation; deficit (24): up to midline but not beyond it; and deficit (25): could not rotate eye from opposite field to midline.5 Magnetic Resonance Imaging Thin-section MRI of the brainstem and the orbit was performed using a 3.0 T system (Siemens Magnetom Verio 3.0, Erlangen, Germany). Scanning was performed to visualize the cisternal segment of CN III and CN VI with a 12-channel head coil using a CISS sequence. Three-D T1 and T2 imaging were performed to assess the other intracranial structures and the extraocular muscles. The parameters of these sequences are as follows: 3D T1: repetition time/echo time (TR/TE) = 1900/2.52 milliseconds, inversion time = 900 milliseconds, FA = 9°, field of view (FOV) = 250 · 250 mm2, 176 sagittal slices, slice thickness = 1 mm, no gap; 3D-CISS: TR/TE = 8.56/3.91 milliseconds, FA = 50°, FOV= 150 · 150 mm2, 64 axial slices, slice thickness = 0.5 mm, no gap; T2: TR/TE = 3,944/98 milliseconds, FA = 150°, FOV= 180 · 180 mm2, 24 coronal slices, slice thickness = 2 mm. The evaluation of MRI was interpreted by 2 oculists who were blinded to the clinical type of DRS in each patient. The results were confirmed by 2 radiologists separately. The diameters of CN III and CN VI were measured at 3 locations (the middle of the cisternal space, 1 section above and below), and the average values were recorded.7 As previously mentioned,6 we considered the image plane in each orbit designated “zero,” which included the globe–optic nerve junction in the central gaze. The EOM cross-sectional area was averaged across subjects in 2 mm thickness referenced to image plane zero. The EOM volume in the orbit was defined as the sum of the EOM areas at the 8 planes multiplied by 2 mm, including the plane “zero” and the planes of 4 mm and 10 mm anterior or posterior to the plane “zero” (shown in Fig. 1). All patients were required to fix a central target except those who were under sedation. Statistical Analyses Statistical analyses were performed by using SPSS software (version 27.0.1 IBM, Armonk, NY). Groups were compared with the paired t test. Pearson and eta correlation coefficients were assessed to determine significant correlations between factors. The results were considered as significant at the level of 0.05. Data are expressed as mean ± SE. RESULTS Patient Characteristics A total of 20 normal subjects of mean age 9.07 ± 2.025 years (range, 1–36 years) were imaged as control. In the Duane syndrome group of 42 patients, the mean age of 5.92 ± 5.02 years (range, 1–32 years). In the overall sample of patients, 20 patients (47.6%) had DRS Type I, 5 patients (12%) had FIG. 1. Magnetic resonance imaging in a patient with Type II DRS. A. Optic nerve–globe junction defined as the plane “zero.99 (B) T2 coronal image of both orbits. 102 Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 Original Contribution Type II, and 17 patients (40.7%) had Type III. There were 36 patients with unilateral DRS and 6 patients with bilateral DRS. Clinical characteristics of subjects are summarized in Supplemental Digital Content 1 (see Tables S1–3, http:// links.lww.com/WNO/A714, http://links.lww.com/WNO/ A715, http://links.lww.com/WNO/A716). Cranial Nerve Features and Changes in Extraocular Muscles Based on Clinical Classification Overall, similar widths of CN III and CN VI were present on both sides among normal controls. Meanwhile, CN III on both sides was intact in all patients with DRS. There was no difference of the width of CN III on both sides in DRS Type II (P = 0.83). However, CN III on the affected side was thicker than that of the nonaffected side in DRS Type I (2.08 ± 0.09 vs 1.75 ± 0.06 P , 0.05) and Type III (2.05 ± 0.06 vs 1.984 ± 0.047 P , 0.05). Regarding the appearance of CN VI, CN VI on the affected side was absent in 24 eyes of 20 patients (100%) with DRS Type I and 16 eyes of 15 patients (88.2%) with Type III. Conversely, CN VI was present in all 6 eyes of 5 patients (100%) with Type II and 2 eyes of 2 patients (11.8%) with Type III. The diameter of CN VI on the affected side was thinner than that of the contralateral side in Type I (0 mm vs 1.14 ± 0.11 mm P , 0.005) and Type III (0.15 ± 0.15 mm vs 1.19 ± 0.07 mm, P , 0.005). Conversely, no difference was found between both sides in Type II DRS (data are summarized in Table 1). Cross-sectional areas of the LR, MR, and SO were measured over an anteroposterior extent from the orbital apex to the globe equator. In all LR muscles, the cross-sectional area, approximately 4 mm posterior to the plane “zero”, was maximal in midorbit.6 The mean maximum LR cross-sectional areas in normal subjects were 35.21 ± 2.40 mm2 (right) and 34.01 ± 2.15 mm2 (left). This area in the affected eye in DRS Type I showed a trend toward being less than that in the nonaffected eye (31.44 ± 1.21 mm2 vs 37.32 ± 2.73 mm2 P , 0.05). No difference was found in the LR maximum cross-sectional area in eyes with Type II (P = 0.94) and Type III DRS (P = 0.17). Because the mean maximum cross-sectional area did not adequately represent the changes in EOM volumes, we further assessed the volume of EOMs to confirm these changes. The affected side LR muscles’ size was thinner than those in the nonaffected side in DRS Type I (381.28 ± 15.43 mm3 vs 410.44 ± 14.92 mm3 P ˂ 0.05) and DRS Type III (374.14 ± 17.41 mm3 vs 406.94 ± 17.10 mm3, P ˂ 0.001), but not in Type II DRS (P . 0.05). The maximum MR cross-sectional areas were 21.72 ± 0.84 mm2 (right) and 23.08 ± 0.13 mm2 (left) in normal subjects approximately 2 mm posterior to the plane “zero”. For DRS Type I, this area of the affected eye was larger than that of the nonaffected eye (21.97 ± 1.30 mm2 vs 19.23 ± 1.37 mm2, P , 0.05); there was no difference of maximum MR cross-sectional area in Type II (P = 0.55) and Type III DRS (P = 0.26). The MR volumes were larger in the Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 affected eye with Type I (285.12 ± 14.50 mm3 vs 261.88 ± 13.68 mm3 P ˂ 0.05) and Type III (288.66 ± 13.67 mm3 vs 263.14 ± 10.15 mm3 P ˂ 0.05), but not in Type II DRS (P= 0.30). The maximum SO cross-sectional areas were 9.07 ± 0.74 mm2 (right) and 9.07 ± 0.74 mm2 (left) in normal controls approximately at the plane “zero”. No changes were found between the affected eye and the nonaffected eye among DRS Type I (P = 0.77), Type II (P = 0.40), and Type III (P = 0.44). All data are shown in Supplemental Digital Content 2 (see Table S4, http://links.lww.com/ WNO/A717), Figure 2. Cranial Nerve Features and Changes in Extraocular Muscles Based on the Presence of Abducens Nerves Imaging features of the cranial nerve and EOMs were compared between groups according to the presence of CN VI. In the absent group, the diameter of CN III on the affected side was thicker than that of the nonaffected side (2.05 ± 0.06 mm vs 1.82 ± 0.06 mm P , 0.05). The maximum LR cross-sectional area and LR volume were smaller in the affected eye than in the nonaffected eye (30.59 ± 1.11 mm2 vs 33.84 ± 1.88 mm2, P , 0.05; 366.54 ± 10.86 mm3 vs 401.37 ± 12.08 mm3 P , 0.05). Simultaneously, the maximum MR cross-sectional area and MR volume were both larger in the affected eye than in the nonaffected eye (21.36 ± 0.79 mm2 vs 20.15 ± 0.89 mm2 P , 0.05; 281.34 ± 9.22 mm3 vs 260.19 ± 8.78 mm3 P = 0.007). Moreover, no differences in the maximum SO cross-sectional area and SO volume were noted on both sides (P = 0.29, P = 0.22). In the present group, there were no differences between 2 eyes regarding oculomotor diameter (P= 0.49); maximum LR, MR, and SO cross-sectional area; and MR, LR, and SO volumes (P = 0.17, P = 0.34, P = 0.4; P = 0.76, P = 0.34, and P = 0.16, respectively, shown in Fig. 3 and presented in Table 2, See Supplemental Digital Content, Table S5, http://links.lww. com/WNO/A718). We analyzed the structure–function relationship among the CN VI, horizontal recti, and ocular motility. The presence of CN VI was correlated with better abduction (E2 = 0.47 P = 0.008). However, no correlation was noted between the range of adduction and LR/MR ratio as well as the abduction and LR volume in patients with or without an abducens nerve. Interestingly, in the absent group, a positive correlation was observed between the CN III diameter and LR volume (r = 0.567 P = 0.007) and MR volume (r = 0.517, P = 0.016) in the affected eye. Instead, no associations were found between the CN III diameter and horizontal rectus muscle volumes on both sides in the present group. DISCUSSION We investigated the morphology of CN III and CN VI as well as evaluated the EOM sizes in normal subjects and 103 Original Contribution TABLE 1. Diameters of CN III and CN VI in patients with Duane retraction syndrome (DRS) according to their clinical classification Total N = 36 Type 1 N = 16 Type 2 N=4 Type 3 N = 16 Controls N = 20 Cranial Nerve (CN) Affected Eye Right Eye (Control) (mm) Nonaffected Eye Left Eye (Control) (mm) P* CN III CN VI CN III CN VI CN III CN VI CN III CN VI CN III CN VI 2.05 ± 0.05 0.238 ± 0.096 2.08 ± 0.09 0 1.90 ± 0.12 1.05 ± 0.0 2.05 ± 0.066 0.15 ± 0.15 2.06 ± 0.052 1.38 ± 0.062 1.82 ± 0.06 1.15 ± 0.05 1.75 ± 0.06 1.14 ± 0.11 1.53 ± 0.05 1.05 ± 0.0 1.984 ± 0.047 1.19 ± 0.07 2.04 ± 0.05 1.36 ± 0.054 ,0.05 ,0.05 ,0.05 ,0.05 0.83 .0.05 ,0.05 ,0.05 .0.05 .0.05 Subjects with bilateral DRS were excluded during analysis. *P , 0.05. patients with DRS. Furthermore, we assessed the structure– function relationship of the horizontal rectus volume and CN VI on ocular motility. According to the clinical classification, CN VI was absent in all patients with Type I and most patients with Type III DRS but present in all patients with Type II and a few patients with Type III DRS. Thicker CN III of the affected side, combined with smaller LR muscles and larger MRs, was found in patients with Type I and Type III DRS. Based on the presence of CN VI, thicker CN III diameters, smaller LR muscles, and larger MRs were found in the affected eyes in the CN VI absent groups. In addition, the LR and MR volumes have positive correlations with CN III diameter in the affected side in the absent group. Finally, the presence of CN VI was correlated with better abduction. FIG. 2. Mean lateral rectus muscle cross-sectional areas and volumes in central gaze of patients with Duane retraction syndrome according to clinical classification. LR affect: LR affect side; LR non affect: LR non affect side; MR affect: MR affect side; MR non affect: MR non affect side; Normal: control group. Bar graph stands for volumes in central gaze of patients with DRS. Line graph stands for mean lateral rectus muscle cross-sectional areas. Yellow color: non-affect side; blue color: affect side. *P , 0.05. 104 Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 Original Contribution FIG. 3. Mean lateral rectus muscle cross-sectional area and volumes in central gaze of patients with Duane retraction syndrome according to the presence of the abducens. LR affect: LR affect side; LR non affect: LR non affect side; MR affect: MR affect side; MR non affect: MR non affect side; Normal: control group. Bar graph stands for volumes in central gaze of patients with DRS. Line graph stands for mean lateral rectus muscle cross-sectional areas. Yellow color: non-affect side; blue color: affect side. *P , 0.05. Different pathologies of DRS have been widely studied. The absence of CN VI on the affected side of DRS Type I was reported by some researchers.2,4,7 Conversely, Kim JH suggested that CN VI is present in patients with Type II DRS,8 although someone failed to identify the cisternal portion of CN VI in Type II DRS.9 Moreover, the idea that pathology is different between these 2 types of DRS put forward Type III DRS. Previous studies evaluated patients with Type III DRS with the variable presence of CN VI.2–4,10 Yang believed that Type I and Type III DRS shared the same pathophysiology, such as the common absence of CN VI in the 2 types of DRS.10 Using electromyography, different types of anomalous lateral rectus muscle innervations in DRS Type I and Type III have been recorded by reason of the variable amount of the CN III fibers for supply to the lateral rectus.11 Our findings are in agreement with their opinions.2,4,7 The subtle difference was that patients with absent CN VI accounted for most of these in Type III DRS. We considered that DRS types I and III may be recognized as a continuum. TABLE 2. Diameters of CN III and CN VI in patients with Duane retraction syndrome (DRS) according to the presence of CN VI Total N = 36 Absent CN VI N = 29 Present CN VI N=7 Controls N = 20 Cranial Nerve (CN) Affected Eye Right Eye (Control) (mm) Nonaffected Eye Left Eye (Control) (mm) P* CN III CN VI CN III CN VI CN III CN VI CN III CN VI 2.05 ± 0.05 0.238 ± 0.096 2.05 ± 0.06 0 2.04 ± 0.11 1.05 ± 0.02 2.06 ± 0.052 1.38 ± 0.025 1.82 ± 0.06 1.15 ± 0.05 1.93 ± 0.05 1.13 ± 0.05 1.62 ± 0.07 1.18 ± 0.08 2.04 ± 0.05 1.36 ± 0.024 ,0.05 ,0.05 ,0.05 ,0.05 0.83 .0.05 .0.05 .0.05 Subjects with bilateral DRS were excluded during analysis. *P , 0.05. Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 105 Original Contribution According to our observation, the presence of CN VI might be related to improved abduction, but not be direct evidence of its normal function. The paradoxical synergistic innervation results in anomalous recruitment of the LR on intended adduction, perhaps complicated by secondary mechanical changes in extraocular muscles.6,11,12 Thus, DRS is probably a disease of anatomical and innervational disorders.3,11,12 Hence, we evaluated the morphology of CN III and the EOMs, providing indirect evidence of aberrant innervation. MRI findings showed that the inferior division of CN III innervated the LR anomalously as it enters the orbit accompanied by CN VI.3 Compensatory thickening of CN III of the affected eye was found in patients with DRS types I and III and all patients with DRS without CN VI. This is in line with a previous study showing that CN III was thicker in patients with DRS with absent CN VI.11,13 Furthermore, the CN III width has a positive correlation with LR volume in the affected eye referring only to the absent group, supporting the idea that a widespread regeneration of CN III innervates the LR in the absent group. Further pieces of evidence support the above points. First, smaller LR volumes were shown in the absent group and patients with DRS Types I and III. It is easy to understand that LR hypoplasia of the affected eye is due to lack of normal innervation by the abducens.10,13 By contrast, Özkan could not find any changes in the horizontal recti size.14 Kang and Demer found that patients with DRS exhibited no extraocular muscle hypoplasia.6,15 Possible explanations for different outcomes are as follows: first, different measurements in horizontal recti were used. The weakness of the width and cross-sectional area of EOMs in 2D may induce some bias in the evaluation and could not represent the size of EOMs entirely; second, no subgroup analyses were performed; and next, larger MR volumes of the affected eye were observed in the absent group and patients with DRS Types I and III. It is noteworthy to mention that long-term LR atrophy is always accompanied by agonistic muscle (MR) contracture, which is opposite to Kang’s perspective.6 In addition, compensated changes of CN III might play another role in neurotrophic support for the medial rectus. Meanwhile, no SO change was observed in our study, differing from previous findings showing the anterior hypoplasia of the superior oblique muscle.3 Finally, in challenge to previous findings, we found that there was no correlation between the relative ratio of LR/ MR volume and adduction as well as LR volume and abduction either in the absent or present group, partially due to small sample size and different criteria for ocular movement. There are several limitations to our study, including its relatively small size, retrospective study, indirect evidence of aberrant innervation, and patients without fixation controlling who were under sedation. In summary, we investigated different pathologies on DRS with characteristic appearances of CN VI and CN III on MRI. Horizontal rectus have morphological changes to adapt to dysinnervation of CN VI and aberrant innervation of CN III. 106 Our results indicate that the use of MRI provides a new diagnostic criterion for the classification of DRS and leads to further comprehension of the pathophysiology of DRS. See Supplemental Digital Content, Figures S1, S2, and S3, http://links.lww.com/WNO/A711, http://links.lww. com/WNO/A712, http://links.lww.com/WNO/A713. STATEMENT OF AUTHORSHIP Conception and design: Y. Guo, W. Zhang, K. Zhao, Q. Zhang; Acquisition of data: T. Zhang, L. Guo, S. Liu, Q. Zhang; Analysis and interpretation of data: Y. Guo, T. Zhang. Drafting the manuscript: Y. Guo, T. Zhang; Revising the manuscript for intellectual content: W. Zhang, K. Zhao. Final approval of the completed manuscript: Y. Guo, W. Zhang, Q. Zhang. REFERENCES 1. Huber A. Electrophysiology of the retraction syndromes. Br J Ophthalmol. 1974;58:293–300. 2. Kim JH, Hwang JM. Presence of the abducens nerve according to the type of Duane’s retraction syndrome. Ophthalmology. 2005;112:109–113. 3. Xia S, Li RL, Li YP, Qian XH, Chong V, Qi J. MRI findings in Duane’s ocular retraction syndrome. Clin Radiol. 2014;69:e191–e198. 4. Taglialatela G, Conforti R, Notaro M, Cotticelli L, Caranci F, Cirillo S. Role of magnetic resonance imaging in Duane’s retraction syndrome: presence of the abducens nerve depending on type. A clinical-anatomical study. Neuroradiol J. 2010;23:704–706. 5. Scott AB, Kraft SP. Botulinum toxin injection in the management of lateral rectus paresis. Ophthalmology. 1985;92:676–683. 6. Kang NY, Demer JL. Comparison of orbital magnetic resonance imaging in duane syndrome and abducens palsy. Am J Ophthalmol. 2006;142:827–834. 7. Parsa CF, Grant PE, Dillon WJ, du Lac S, Hoyt WF. Absence of the abducens nerve in Duane syndrome verified by magnetic resonance imaging. Am J Ophthalmol. 1998;125:399–401. 8. Kim JH, Hwang JM. Abducens nerve is present in patients with type 2 Duane’s retraction syndrome. Ophthalmology. 2012;119:403–406. 9. Denis D, Dauletbekov D, Girard N. Duane retraction syndrome: type II with severe abducens nerve hypoplasia on magnetic resonance imaging. J AAPOS. 2008;12:91–93. 10. Yang HK, Kim JH, Hwang JM. Abducens nerve in patients with type 3 Duane’s retraction syndrome. PLoS One. 2016;11:e150670. 11. Yüksel D, Orban DXJ, Lefèvre P. Review of the major findings about Duane retraction syndrome (DRS) leading to an updated form of classification. Vision Res. 2010;50:2334–2347. 12. Hoyt WF, Nachtigäller H. Anomalies of ocular motor nerves. Neuroanatomic correlates of paradoxical innervation in Duane’s syndrome and related congenital ocular motor disorders. Am J Ophthalmol. 1965;60:443–448. 13. Yang HK, Kim J, Lee DS, Hwang JM. Association of lateral rectus muscle volume and ocular motility with the abducens nerve in Duane’s retraction syndrome. Graefes Arch Clin Exp Ophthalmol. 2021;259:205–211. 14. Özkan SB, Arıbal ME. Comparison of orbital magnetic resonance imaging in Duane syndrome and abducens palsy. Am J Ophthalmol. 2007;143:907. 15. Demer JL, Ortube MC, Engle EC, Thacker N. Highresolution magnetic resonance imaging demonstrates abnormalities of motor nerves and extraocular muscles in patients with neuropathic strabismus. J AAPOS. 2006;10:135–142. Guo et al: J Neuro-Ophthalmol 2024; 44: 101-106 |
