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Show ORIGINAL CONTRIBUTION Ocular Misalignment in Graves Disease May Mimic That of Superior Oblique Palsy Vicki M. Chen, MD and Linda R. Dagi, MD Background: The Parks-Bielschowsky three-step test (TST) can incorrectly indicate that a superior oblique muscle is paretic in patients with restrictive strabismus. Although this pitfall in diagnosis has been widely reported, no large studies have examined the incidence of a positive TST in patients with Graves disease. Methods: We performed a retrospective chart re-view of 31 consecutive patients with Graves orbitopathy examined at Children's Hospital of Boston from 2003 to 2007. We analyzed ocular ductions, misalignment, and torsion, and thyroid function studies. Results: Six (20%) of the patients had a positive TST, 3 (10%) of which showed excyclotorsion in at least one eye. However, of the 6 patients, 5 had obvious ocular adnexal signs of Graves disease and 2 had obvious supraduction deficits, leaving only 1 (3%) patient in whom the clinician would have mistakenly diagnosed a superior oblique palsy. Conclusions: Although a positive TST occurs frequently in Graves disease, other clinical features should allow distinction from superior oblique palsy in most patients. (J Neuro-Ophthalmol 2008;28:302-304) Apositive Bielschowsky-Parks three-step test (TST) is traditionally interpreted as implicating a single paretic cyclovertical muscle (1), usually the superior oblique muscle. Traditional paradigms direct the surgeon to weaken the ipsilateral inferior oblique muscle or the contralateral inferior rectus muscle or to strengthen the ipsilateral superior oblique muscle (2). However, restrictive myopathies, including Graves disease, can cause a positive TST and have been reported to mimic superior oblique palsy (3,4). In early Graves disease, Department of Ophthalmology, Children's Hospital Boston, Boston, Massachusetts. Address correspondence to Vicki M. Chen, MD, Department of Pediatric Ophthalmology, New England Eye Center, 800 Washington Street, Box 450, Boston, MA 02111, E-mail: vchen@tuftsmedicalcenter.org findings of lid retraction or exophthalmos are not always clinically evident. If these soft tissue signs of Graves orbitopathy are subtle or absent, the finding of a positive TST may direct the surgeon to mistakenly diagnose a superior oblique palsy. Subsequent erroneous surgical treatments have the potential to cause disabling vertical and torsional diplopia. Although this pitfall in diagnosis has been widely reported, no large studies have examined the incidence of a positive TST in patients with Graves disease. To address this issue, we performed a retrospective study. METHODS The medical and ophthalmologic records of all patients with Graves disease evaluated in the senior author's strabismus practice between 2003 and 2007 were reviewed. The diagnosis of Graves disease was based on clinical findings typical for hyperthyroidism and thyroid function studies, including elevated thyroxine (T4), triiodothyronine (T3), or free T4, suppressed thyrotropin (TSH), positivity of TSH receptor antibodies (TBII), classic features of Graves orbitopathy, and confirmatory imaging documenting tendon-sparing enlargement of involved extraocular muscles. Each patient was evaluated by prism and cover testing with fixation on a distant target. The misalignment of the eye was measured in prism-diopters (PD) in primary gaze, ipsilateral and contralateral side gaze, and ipsilateral and contralateral head tilt positions. Ductional excursions were noted in each patient. Excyclotorsion was measured using the double Maddox rod in a trial frame with the patient fixating on a light source located at a distance of 1 m. The patient was asked to adjust the Maddox rod orientation over each eye, and the degrees of torsion were recorded from the trial frame. The total torsion was calculated by adding the torsional measurements from each eye. Forced ductions were performed only on patients who underwent surgery. An on-line PubMed literature review from 1935 to 2007 was performed using the following keywords: three-step test, Bielschowsky, Bielschowsky-Parks, and Graves disease. Patients with known or suspected neurologic disease, cranial nerve palsies, or prior strabismus surgery were excluded from the study. 302 J Neuro-Ophthalmol, Vol. 28, No. 4, 2008 Ocular Misalignment in Graves Disease J Neuro-Ophthalmol, Vol. 28, No. 4, 2008 RESULTS Thirty-one patients aged between 19 and 74 years were included. There were 19 women and 11 men. Six (20%) patients had a positive TST, and 3 (10%) had excyclotorsion in at least one eye. Five of these 6 patients demonstrated ocular adnexal signs of mild Graves orbitopathy (2 with unilateral proptosis of 2 mm, 2 with lid retraction, and 1 with boggy edema of the lower eyelids bilaterally). The single patient (3% of the cohort) who had a positive TST and excyclotorsion without such adnexal signs had a preliminary diagnosis of a superior oblique palsy. Of those patients with a positive TST, the average hypertropia (HT) was 7 PD in primary gaze, 17 PD on contralateral side gaze, and 12 PD on ipsilateral head tilt. Two of the 6 patients with a positive TST (33%) had a significant supraduction deficit of the hypotropic eye, strongly suggestive of restrictive strabismus. When torsion was present, the involved eye was always excyclotorted. The total torsion averaged 3 degrees. Three of the six patients with a positive TST (50%) demonstrated excyclo-torsion that was greater in the hypertropic eye. Torsional misalignment in head tilt positions was not available for analysis. DISCUSSION Although the incidence of a positive TST was 20% in this study, the diagnosis of Graves disease was apparent in all but one patient (3%) on the basis of adnexal features of mild thyroid orbitopathy and clinical or biochemical manifestations of dysthyroidism. Our finding of excyclo-tropia in 50% of patients with Graves orbitopathy is in accord with that of Caygill (5), who found that 43% of patients had excyclotropia by the Maddox rod test, and that of Trobe (6), who found that 8 (55%) of 15 patients had excyclotorsion greater than 5. Bielschowsky (4) and Kushner (3) have highlighted the possibility of error in the diagnosis of superior oblique palsy. Kushner (3) reported 7 patients with a positive TST who did not have a superior oblique palsy, only one of which had Graves orbitopathy. Metz (7) also reported that restrictive orbitopathy may mimic cranial nerve palsies but did not document whether Graves disease was one of those restrictive entities. FIG. 1. Proposed mechanism for a positive TST in Graves disease with restricted left inferior rectus muscle. A. Schematic version, left eye fixing. Right hypertropia is present in primary gaze due to a restrictive left inferior rectus muscle. The right hypertropia increases in contralateral side gaze because of the increased tone of the left inferior rectus muscle in left gaze. On ipsilateral head tilt, the increased tone of the left inferior rectus results in substantial infraduction, thereby increasing the right hypertropia and also causing excyclotorsion. B. Clinical version, left eye fixing. There is a right hypertropia due to a restrictive left inferior rectus muscle. C. Schematic version, right eye fixing. There is a right hypertropia in primary gaze due to a restrictive left inferior rectus muscle. The right hypertropia increases in contralateral side gaze because of the increased tone of the left inferior rectus muscle in left gaze. On ipsilateral head tilt, the increased tone of the left inferior rectus results in substantial infraduction, thereby increasing the right hypertropia and also causing excyclotorsion. D. Clinical version, right eye fixing. There is a right hypertropia due to a restrictive left inferior rectus muscle. 303 J Neuro-Ophthalmol, Vol. 28, No. 4, 2008 Chen and Dagi Moster et al (8) described 6 patients with a positive TST in whom hyperthyroidism was eventually diagnosed. The mechanism by which Graves disease caused a positive TST was not discussed. We propose a mechanism based on recent physio-logic force-tension studies (9,10) in patients with Graves disease. The steady-state tension (Fs) was significantly higher in patients with more advanced Graves disease than in patients with milder disease. We propose that a positive TST occurs because of increased tension in the involved muscle (Fig. 1). The inferior rectus muscle is the most common vertical rectus muscle affected in Graves orbitopathy. The unilateral infiltration of one inferior rectus or the asymmetric involvement of both inferior recti would result in the following pattern of deviation. The increased tone of the more active inferior rectus in one eye may cause a contralateral hypertropia. On gaze contralateral to the hypertropic eye, the hypotropic eye is placed in abduction, and the inferior rectus is in a position to exert maximal force of contraction, resulting in greater vertical mis-alignment than is seen on gaze ipsilateral to the hypertropic eye. On gaze ipsilateral to the hypertropic eye, the hypotropic eye is placed in adduction, and the inferior rectus is only weakly activated, resulting in less vertical misalignment than is seen on gaze contralateral to the hypertropic eye. On head tilt ipsilateral to the hypertropic eye, excyclotorsion is stimulated in the hypotropic eye, and the inferior rectus, with greater tone, increases the observed vertical misalignment. On head tilt contralateral to the hypertropic eye, intorsion is stimulated in the hypotropic eye, which does not activate the inferior rectus muscle of the hypotropic eye. The vertical misalignment would therefore appear greater on head tilt ipsilateral to the hypertropic eye than on head tilt contralateral to the hyper-tropic eye. Figure 1A, C illustrates the mechanism of a positive TST in patients with Graves orbitopathy. The diagrams are shown with left and right eye fixing, respec-tively, to demonstrate the variation in clinical presentation. Illustrative clinical photos are shown in Figure 1B, D. As unilateral or bilateral and asymmetric inferior rectus enlargement is a common finding in Graves orbitopathy and a frequent occurrence in the setting of vertical misalignment with this disorder, our model suggests that a predictably high percentage of patients with vertical misalignment in this condition will have a positive TST. The most common surgical treatment for superior oblique palsy is ipsilateral inferior oblique weakening. This procedure would not typically be the surgical approach chosen to remedy vertical misalignment due to Graves orbitopathy and might exacerbate vertical and torsional misalignment. Orbital imaging, clearly helpful in di-agnosing early Graves orbitopathy, may not be considered in cases of presumed isolated superior oblique palsy. Its absence might delay the correct diagnosis. REFERENCES 1. Parks MM. Isolated cyclovertical muscle palsy. AMA Arch Ophthalmol 1958;60:1027-35. 2. Knapp P, Moore S. Diagnosis and surgical options in superior oblique surgery. Int Ophthalmol Clin 1976;16:137-49. 3. Kushner BJ. Errors in the three-step test in the diagnosis of vertical strabismus. Ophthalmology 1989;96:127-32. 4. Bielschowsky A. Lectures on motor anomalies of the eyes: II. Paralysis of individual eye muscles. Arch Ophthalmol 1935;13: 33-59. 5. Caygill WM. Excyclotropia in dysthyroid ophthalmopathy. Am J Ophthalmol 1972;73:437-41. 6. Trobe J. Cyclodeviation in acquired vertical strabismus. Arch Ophthalmol 1984;102:717-20. 7. Metz HS. Restrictive factors in strabismus. Surv Ophthalmol 1983; 28:71-83. 8. Moster ML, Bosley TM, Slavin ML, Rubin SE. Thyroid ophthalmopathy presenting as superior oblique paresis. J Clin Neuroophthalmol 1992;12:94-7. 9. Tian S, Bolzani R, Benassi M, Lennerstrand G. Eye muscle force development in thyroid-associated ophthalmopathy in different stages of disease. Acta Ophthalmol Scand 2007;85:431-7. 10. Simonsz HJ, Kommerell G. In Graves disease, increased muscle tension and reduced elasticity of affected muscles is primarily caused by active muscle contraction. Neuroophthalmology 1989;9:243-5. 304 q 2008 Lippincott Williams & Wilkins |
