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J Med Dent Sci 2010； 57： 75－82

Original Article

Prevalence of Strabismus in Patients with Pathologic

Akiko Tanaka, Kyoko Ohno-Matsui, Noriaki Shimada, Kengo Hayashi, Yuko Shibata, Takeshi Yoshida, Makiko Yamashita, Takashi Tokoro and Manabu Mochizuki

Department of and Visual Science, Tokyo Medical and Dental University Graduate School

Background: To determine the prevalence and clinical features of strabismus in patients with Introduction pathologic myopia. Methods: Medical records of a total of 636 highly Pathologic myopia is one of the major causes of myopic patients were retrospectively reviewed. blindness worldwide. [1, 2] Pathologic myopia Pathologic myopia was defined as spherical reportedly causes not only pathological complications, equivalent (SE) of at least -8D, or axial length such as , and >26.5 mm in patients older than 9 years, <-4D in optic disc abnormalities, [3] but also functional those younger than 5 years, <-6D in those aged problems, such as misalignment of position. from 6 to 8 years. Myopic refractive degree, axial According to our clinical experience, horizontal and/or length measurements, best-corrected vertical strabismus is often observed in patients with and eye position were then analyzed. pathologic myopia. In Curtin’s review of the motility Results: Among 636 patients with pathologic clinic, high myopia was disproportionately frequent myopia, 520 (81.8%) had orthophoria, 85 (13.4%) when compared to lower grades in every classification had and 31 (4.9%) had at near of horizontal tropia, [4] but vertical strabismus was not distance. At long distance, 499 (86.5%) had discussed. To the best of our knowledge, there have orthophoria, 51 (8.8%) had exotropia and 27 been no previous studies describing the general (4.7%) had esotropia. Vertical heterotropia was characteristics of eye position in high myopes. seen in 103 patients (16.2%). The mean axial Progressive esotropia is known in high myopes. length was significantly longer and the mean age Hugonnier and Magnard were the first to direct was higher in esotropia than orthophoria and in attention to restrictive motility disturbances in severe patients with vertical heterotropia than without myopia. [5] Esodeviation in high myopia was estimated vertical heterotropia. There were 16 patients with to be an acquired condition, and progressed into myopic strabismus fixus or acquired progressive convergent strabismus and, in severe cases, myopic esotropia. strabismus fixus. One cause of progressive esotropia Conclusions: This study confirmed the relatively is the disproportional size of the and the volume of high prevalence of horizontal and vertical an elongated eyeball due to pathologic myopia, which strabismus in patients with pathologic myopia. may be secondary to displacement of the lateral rectus muscle pulley system. [6] As surgical treatment of Key Words: pathologic myopia, , strabismus, myopic strabismus fixus is challenging, numerous axial length studies have reported surgical outcomes. Options for correction range from conventional combined recession-resection surgery to innovative surgical Corresponding Author: Kyoko Ohno-Matsui, MD procedures aimed at correcting the deviated muscle Tokyo Medical and Dental University Graduate School, 1-5-45, paths. [6-10] Yushima, Bunkyo-ku, Tokyo 113-8519, Japan To our knowledge there is little information regarding Tel: +81-3-5803-5302 Fax: +81-3-3811-7188 E-mail: [email protected] the general clinical features of strabismus in high Received September 30；Accepted November 13, 2009 myopes. This study was therefore designed to 76 A. Tanaka et al. J Med Dent Sci investigate the prevalence of horizontal and vertical performed with the JMP software package (SAS strabismus, including acquired progressive esotropia Institute, Cary, NC, USA), version 8. and myopic strabismus fixus in high myopes, and to analyze the relationship between prevalence, patient Results age and axial length. In the present study, we analyzed A total of 1,213 medical records from the High Myopia eye position in a large number of highly myopic Clinic from January 1989 to July 2009 were reviewed, patients, and demonstrated that the prevalence of and 636 of these met the inclusion criteria. Among horizontal/vertical strabismus is high in these patients. these, 588 patients had high myopia bilaterally, and 48 We also demonstrated that prevalence increased with had unilateral high myopia. The clinical characteristics patient age and axial length. of these patients are shown in Table 1. In all, 94 patients had surgery, 35 Patients and Methods showed and 147 eyes showed pseuophakia. Medical records of patients with pathologic myopia Nine underwent operation for retinal detachment. (spherical equivalent (SE) of at least -8D, or axial length Three patients had undergone , >26.5 mm in patients older than 9 years, <-4D in astigmatic keratotomy, photorefractive keratotomy and patients younger than 5 years, <-6D in patients aged radial keratotomy. Two patients had , one from 6 to 8 ), who were examined in our high myopia had and one had microcornea. Twelve clinic at Tokyo Medical and Dental University Hospital patients had a history of surgeries against strabismus. between January 1989 and July 2009, were Although past history of could have biased retrospectively analyzed. [11] the results, all patients were included in order ensure Patients who had records on routine ophthalmic that acquired progressive myopia/myopic strabismus examination, including SE or axial length measurements, fixus patients who often underwent best-corrected visual acuity (BCVA) and eye position were not excluded. examination were enrolled. Cycloplegic autorefraction was performed in all 1. Eye position children aged less than 12 years, and with 2 sets of 1% eyedrops were used. Axial In all eligible patients, at near distance, 520 (81.8%) length was measured with an Alpha II Biometric Ruler had orthophoria, 85 (13.4%) had exotropia, and 31 (Storz Instrument Company, St. Louis, MO, USA), (4.9%) had esotropia. At long distance, 499 (86.5%) Ultrascan (Alcon Laboratories Inc., Fort Worth, TX, USA) had orthophoria, 51 (8.8%) had exotropia and 27 (4.7%) or IOLMaster (Carl Zeiss, Jena, Germany). BCVA was had esotropia. Vertical heterotropia was seen in 103 measured using a Landolt ring chart at a distance of (16.2%) patients. The relationship between age and basically 5 m and expressed as a decimal visual acuity. horizontal eye potion at long distance is shown in The prism and was used to diagnose Figure 1. The relationship between axial length of the strabismus at long distance (5 m) and near distance larger eye and horizontal eye position at long (33 cm) fixation with or contact lenses for best distance is shown in Figure 2. The mean axial length correction. was significantly longer in esotropia (mean: 30.8mm ± 1.7) For patients whose central vision was disturbed due than in orthophoria ((mean 29.1mm ± 1.9, p<0.001), in to myopic chorioretinal atrophy, eye position was esotropia than in exotropia (mean: 29.7mm ± 2.3, examined by Krimsky test using a reflex at near p=0.002) and in exotropia than in orthophoria distance (Krimsky test was not performed at long (p=0.0273). The mean age of patients with esotropia distance). and were included in (mean: 48.7 years old ± 16.5) was significantly higher orthophoria in this study. than in those with orthophoria (mean: 42.4years old ± This study was approved by the Tokyo Medical and 17.5 P=0.0054). In addition, the mean age of patients Dental University Ethics Committee. with vertical heterotropia (mean: 48.7 years old ± 15.9) was significantly higher than in those without vertical Statistics heterotropia (42.7 years old ± 17.8 p=0.0013). The For statistical analysis, the change in drift within the mean axial length in patients with vertical heterotropia eye position of each group was assessed by one-way (mean: 30.4mm ± 2.2) was significantly greater than in analysis of variation (one-way ANOVA) and Wilcoxon/ those without vertical heterotropia (mean: 29.1mm ± 1.9, Kruskal-Wallis analysis. All statistical analyses were p<0.0001). The variations in age and axial length, with Strabismus in Pathologic Myopia 77

Table 1. Patient characteristics.

Characteristics of patients Gender No. patients 636 Men 216 Women 420 Age (y/o), mean (SD) (range) 43.4 ± 17.6（3～ 86） Axial length (mm), mean (SD) (range) 28.7 ± 2.1（21.7～ 36.1） High myopia No. patients Bilateral 588 Unilateral 48 status No. patients bilateral phakia 542 aphakia / pseudophakia 94 y/o; year old, SD; standard deviation or without vertical heterotropia, are shown in Figure 3. have been suggested to be different in Asian and As visual acuity may affect eye position, we further Western populations. [15, 19-23] We found two reports analyzed eye position in 206 patients whose BCVA was that focused on non-pediatric patients; the prevalence

＞－1.0 in both eyes. Their age ranged from 5 to 77 of strabismus was 3.6% and 5% [24, 25] In the present years (mean: 33.26 ± 14.5 years); 110 (53.0%) were study, the prevalence of horizontal strabismus was women and 96 (47.0%) were men. In this group, 14 found to be 18.3% at near distance and 13.5% at long (6.8%) patients had exotropia, 2 (1.0%) had esotropia at distance. The large prevalence discrepancies in high near distance, and 16 (7.8%) had vertical heterotropia. myopes when compared to other reports suggest that Unilateral high myopia was found in 48 patients, 15 the prevalence of horizontal strabismus is very high, (35.7%) patients had exotropia, 3 (7.1%) patients had which suggests a strong relationship between esotropia at near distance and 9 (18.8%) had vertical pathologic myopia and horizontal strabismus. Visual heterotropia. impairment and visual field defects due to pathological complications of high myopia may decrease fusion and 2. Myopic strabismus fixus/ may induce off-balanced eye positioning. Sensory Acquired progressive esotropia esotropia/exotropia can be one reason to increase horizontal strabismus in aged pathologic myopia. When medical records referred to progressive With regard to the ratio of exotropia and esotropia esotropia which did not previously exist, the patient among horizontal strabismus, our results showed similar was diagnosed as having acquired progressive patterns as population-based Asian reports; exotropia esotropia. Large esohypotropia with limited motility was 2.74 times more frequent than esotropia at near was diagnosed as myopic strabismus fixus. There were distance and for all age groups, exotropia was more 6 cases of acquired progressive esotropia and 10 common than esotropia. Glasses or contact lenses for cases of myopic strabismus fixus. Ten patients were high myopes are often under correction for their too referred to the strabismus clinic of our hospital and strong . These conditions inferentially were confirmed by further tests and diagnostic imaging. induce less and exotropia. Clinical characteristics of these patients are The present study also clarified a high prevalence of summarized in Table 2. vertical strabismus in patients with pathologic myopia (16.2%). Although epidemiology studies of vertical Discussion strabismus are rare, Tollefson reported its prevalence Many studies reporting the prevalence of strabismus as being 0.26% in a pediatric population-based study. have been limited to children, and the prevalence of [26] Vertical heterotropia in healthy Japanese aged strabismus among children is reportedly 2.4 to 5%. [12- over 60 years was reported as 6%. [27] In our study, 14] Slight differences have been reported among 116 subjects were aged over 60 years and the rate of ethnicity, [12, 15-18] even though strabismus patterns vertical heterotropia in this group was very high at 90 78 A. Tanaka et al. J Med Dent Sci

Figure 1 : Relationship between age and horizontal eye potion at near distance. For all age groups, orthophoria was most common and exotropia was more common than esotropia.

Figure 2 : Relationship between axial length of larger eye globe and horizontal eye position at near distance. In larger axial length group, the rate of orthophoria decreased. Strabismus in Pathologic Myopia 79

Figure 3a : Variations in age with or without vertical heterotropia. Figure 3b : Variations in axial length with or without vertical The mean age of patients with vertical heterotropia heterotropia was significantly higher than those without vertical The mean axial length of patients with vertical heterotropia. heterotropia was significantly longer than those without vertical heterotropia.

Table 2. Clinical characteristics of myopic strabismus fixus and acquired progressive esotropia.

best corrected axial length (mm) visual acuity Age (y/o) Sex right Left right left eye position surgery type of surgery 52 F 30.6 30.4 0.4 1.5 progress - 34 M 31.1 31.1 1 1 progress - 52 M 29.0 29.2 1 1.2 progress - 42 F 31.4 31.1 1.2 1.5 progress + recession 72 F 34 33 0.1 0.3 progress - 49 F 32.4 32.4 0.8 0.5 progress + muscle union 45 F 32.4 32.0 0.5 0.5 fixus + muscle union 69 M 28.8 30.6 0.1 0.5 fixus + muscle union+recession 65 F 32.0 32.0 1.2 0.8 fixus + recession-resection 67 F 28.0 30.3 0.09 0.15 fixus + muscle union+recession 53 F 36.0 33.9 0.6 0.9 fixus + muscle union 47 F 31.3 31.5 0.04 0.3 fixus + muscle union 69 M 36.1 35.6 0.7 0.5 fixus - 76 F 30.0 28.7 0.02 0.06 fixus + muscle union+recession 46 F 31.9 31.2 0.7 0.9 fixus + muscle union+recession y/o；year old fixus=myopic strabismus fixus progress=acquired progressive esotropia 80 A. Tanaka et al. J Med Dent Sci

Table 3. Clinical characteristics of good BCVA group with vertical heterotropia.

axial length (mm) degree of Age (y/o) Sex right left Eye states heterotropia (PD) 50 M 28 29 7 31 M 28 28 2 13 F 25.9 25.8 5 46 F 26.1 26.2 7 28 F 30.5 30.5 3 temporal visual field defect RE 28 M 27.6 27.4 6 27 F 28.1 27.6 4 29 M 28.4 28.5 12 SR under 27 M 29 29 8 58 M 30.9 31.5 6 aphakia BE, temporal visual field defect LE 47 F 31.4 30.8 1 35 M 26.1 26.0 3 13 M 30.8 29.2 4 muscle recession+resection 21 F 29.1 29.4 4 44 M 27.6 27.7 2 retino schisis RE 23 M 29.2 29.3 16 SO palsy LE RE; right eye y/o; year old LE; left eye PD; prizum diopter BE; both eyes SR; superior oblique SO; superior rectus

(20.4%). High myopes have a higher chance of eye size of eyeballs may contribute to unilateral contact surgery due to their eye complications, and these between eyeball and orbital bones or asymmetric visual surgeries may induce vertical heterotropia as a result input may evoke the vertical divergence. of anesthesia, silicon buckle or damage to extraocular Demer et al. recently considered new aspects of the muscle by the surgery itself. Surprisingly, patients with functional anatomy of the orbit, showing that the good BCVA had also high rate (7.8%). We examined the pass through connective tissue details of vertical heterotropia in highly myopic patients sleeves in the posterior Tenon’s fascia; these were with good BCVA and past eye history which may cause termed “pulleys”. [28] Axial myopia may have a milder, heterotropia was found in 6 patients (Table 3). dynamic form of inferior slippage of the lateral rectus Nonetheless, there were ten patients with vertical pulley, thereby causing strabismus. [29] Aoki heterotropia without any other eye problems, except concluded that in acquired progressive myopia, the high myopia and diffuse atrophy in the posterior . lateral rectus shifted inferiorly, while the superior The cause of these heterotropia is unclear as many rectus shifted nasally, but there was no significant other comitant strabismus. dislocation of the extraocular muscle path in high It is also interesting that unilateral group had quite myopes without ocular deviation. [6] It has not been high prevalence of vertical heterotropia as 18.8%. reported whether there were any particular changes in Curtine mentioned that unilateral high myopia is much muscle or pulleys in high myopes with strabismus more common than hyperopia and the strong tendency without restriction of ocular motility. The effects of for were associated with unilateral or aging may cause inferior displacement of the horizontal anisometropic myopia. [4] Although the number of rectus extraocular muscles and corresponding pulleys. unilateral high myopia is limited as 48 in the current [30] This dislocation may enhance the change in study, we found that vertical heterotropia also muscle path in aged high myopes and cause a higher associated with unilateral myopia. A difference of the prevalence of vertical heterotropia. Further Strabismus in Pathologic Myopia 81 investigation into morphology-dependent changes in progressive esotropia caused by high myopia: a new highly myopic eyes may reveal the relationship between surgical procedure based on its pathogenesis. In: de high myopes and eye orientation. Faber JT, ed. Transactions: 27th meeting, European Strabismological Association, Florence, Italy, 2001. Lisee, A limitation in the present study is that this is a non- Netherlands: Sweets & Zeitlinger 2002:145-148 randomized retrospective review, and the patient 10. Krzizok TH, Kaufmann H, Traupe H. New approach in population was based on referrals to a high myopia strabismus surgery in high myopia. Br J Ophthalmol. clinic. The details of strabismus and 1997;81:625-630 were often not described, and some high myopes with 11. Tokoro T. On the definition of pathologic myopia in group strabismus did not seek out referrals to the strabismus studies. Acta Ophthalmol. Suppl. 1988;185:107-108 clinic, as they were not distressed by their eye position 12. Stidwill D. Epidemiology of strabismus. Ophthalmol Physiol Opt. 1997;17:536-539 or , mainly due to their low visual acuity. The 13. Multi-ethnic Study Group. Prevalence of current study revealed a rate of myopic strabismus and strabismus in African American and fixus or acquired progressive esotropia patients of Hispanic children ages 6 to 72 months. Ophthalmol. 2.5%, but few people had their eye positions measured 2008;115:1229-1236 only once and the number of progressive esotropia may 14. Williams C, Northstone K, Howard M, et al. Prevalence have been underestimated. To clarify this issue, a and risk factors for common vision problems in children: prospective study is necessary. data from the ALSPAC study. Br J Ophthalmol. 2008;92:959-964 In conclusion, strabismus was observed at a relatively 15. Matsuo T, Matsuo C. Comparison of prevalence rate of high prevalence in highly myopic patients and should strabismus and amblyopia in Japanese elementary school be regarded as one of the major complications of children between the years 2003 and 2005. Acta Med pathologic myopia. We recommend that eye positions Okayama 2007;61:329-334 be repeatedly assessed over time and that surgical 16. Shrestha RK, Joshi MR, Ghising R, et al. Ocular morbidity procedures be performed as appropriate. among children studying in private schools of Kathmandu valley: A prospective cross sectional study. Nepal Med Coll J. 2006;8:43-46 17. Lu P, Chen G, Zhang W, et al. Prevalence of ocular References disease in Tibetan primary school children. Can J 1. Ghafour IM, Allan D, Foulds WS. Common causes of Ophthlmol. 2008;43:95-99 blindness and visual handicap in the west of Scotland. Br 18. Preslan MW, Novak A. Baltimore Vision Screening J Ophthalmol. 1983;67:209-213 Project. Ophthalmol. 1998;105:150-153 2. Sperduto RD, Seigel D, Roberts J, et al. Prevalence of 19. Yu CB, Fan DS, Wong VM, et al. Changing patterns of myopia in the United States. Arch Ophthalmol. strabismus: a decade of experience in Hong Kong. Br J 1983;101:405-407 Ophthalmol. 2002;86:854-856 3. Saw SM, Gazzard G, Shih-Yen EC, et al. Myopia and 20. Chia A, Roy L, Seenyen L. Comitant horizontal strabismus: associated pathological complications. Ophthal Physiol an Asian perspective. Br J Ophthalmol. 2007;91:1337- Opt. 2005;25:381-391 1340 4. Curtin BJ. Basic Science and Clinical Management. In: 21. Graham PA. Epidemiology of strabismus. Br J Ophthalmol. Ocular Findings and Complications, The Myopias. Harper 1974;58:224-231 & Row Philadelphia, USA. 1985:292-297 22. Govindan M, Mohney BG, Diehl NN, et al. Incidence and 5. von Noorden GK, Campos EC. Special Forms of types of childhood exotropia. A population-based study. Strabismus. In: and Ocular Motility. Sixth Ophthalmol. 2005;112:104-108 edition. Mosby, St Louis USA. 2001:473-474 23. Greenberg AE, Mohney BG, Diehl NN, et al. Incidence and 6. Aoki Y, Nishida Y, Hayashi O, et al. Magnetic resonance types of childhood esotropia. A population-based study. imaging measurements of extraocular muscle path shift Ophthalmol. 2007;114:170-174 and posterior eyeball prolapse from the muscle cone in 24. Nowak MS, Jurowski P, Gos Roman, et al. Ocular findings acquired esotropia with high myopia. Am J Ophthalmol. among young men: a 12-year prevalence study of military 2003;136:484-489 service in Poland. Acta Ophthalmol. EPub ahead of print: 7. Hoerantner R, Kaltofen T, Priglinger S, et al. Model-based 12 May 2009. doi: 10.1111/j.1755-3768.2008.01476.x improvements in the treatment of patients with 25. Adelstein AM, Scully J. Epidemiological aspects of . strabismus and axial high myopia. Invest Ophthalmol Vis Brit Med J. 1967;3:334-338 Sci. 2007;48:1133-1138 26. Tollefson MM, Mohney BG, Diehl NN, et al. Incidence and 8. Sturm V, Menke MN, Chaloupka K, et al. Surgical types of childhood . Ophthalmol. treatment of myopic strabismus fixus: a graded approach. 2006;113:1142-1145 Graefes Arch Clin Exp Ophthalmol. 2008;246:1323-1329 27. Otsuji J, Utsumi T, Yamada A, et al. Distribution of 9. Yokoyama T, Ataka S, Tabuchi H, et al. Treatment of 82 A. Tanaka et al. J Med Dent Sci

vertical eye positioning in the healthy elderly (in 29. Oh SY, Clark RA, Velez F, et al. Incomitant strabismus Japanese, English abstract not available). Ganaka Rinsho associated with instability of rectus pulleys. Invest Iho. 2005;99:554-556 Ophthalmol Vis Sci. 2002;43:2169-2178 28. Demer JL, Miller JM, Poukens V, et al. Evidence for 30. Clark RA, Demer J. Effect of aging on human rectus fibromuscular pulleys of the recti extraocular muscles. extraocular muscle paths demonstrated by magnetic Invest Ophthalmol Vis Sci. 2005;36:1125-1136 resonance imaging. Am J Ophthalmol. 2002;134:872-878