Investigation of fellow eye of unilateral retinal detachment in Shih-Tzu

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1 Veterinary Ophthalmology (2010) 13, 5, Investigation of fellow eye of unilateral retinal detachment in Shih-Tzu Yoshiki Itoh, Seiya Maehara, Ayako Yamasaki, Keiko Tsuzuki and Yasuharu Izumisawa Department of Small Animal Clinical Sciences, School of Veterinary Medicine, Rakuno Gakuen University, 582 Bunkyodai-Midorimachi, Ebetsu, Hokkaido , Japan Address communications to: S. Maehara Tel.: Fax: Abstract Objective To investigate disease in the fellow eye, and consider the relation to rhegmatogenous retinal detachment (RRD) in Shih-Tzus. Animals studied The fellow eyes of 49 Shih-Tzus (27 male, 22 female; median age: 6.8 years) with unilateral RRD diagnosed by funduscopy or ultrasonography at Rakuno Gakuen University Teaching Animal Hospital were assessed in this study. Procedures Ophthalmic examinations (including menace response, pupillary light reflex, slit-lamp biomicroscopy, and funduscopy) were performed in the subjects. Electroretinography was performed in 12 eyes that developed retinal degeneration. Maximum follow-up period was 42 months. Results Cataracts and vitreous opacity were observed in 26 (53%) and 32 eyes (65%), respectively, by slit-lamp biomicroscopy. Retinal degeneration with various degrees of hyper-reflectivity of the tapetal fundus and/or attenuation of retinal vessels was observed in 35 eyes (71%) on funduscopy. A reduction of amplitude in rod, standard combined and 30 Hz flicker electroretingram was detected in 5 (42%), 10 (83%), and 6 eyes (50%), respectively. During the follow-up period, RRD was detected in six eyes. Conclusion Retinal degeneration was frequently detected by funduscopy and electroretingrams in the fellow eye in Shih-Tzus with RRD. In our subjects, vitreous degeneration was also observed frequently. It has been reported that peripheral retinal degeneration is one of the causes of RRD associated with vitreous degeneration in humans. We assume that primary retinal degeneration with secondary vitreous degeneration is one of the causes of RRD in Shih-Tzus. Key Words: electroretinogram, fellow eye, retinal degeneration, retinal detachment, Shih-Tzu, vitreous degeneration INTRODUCTION Retinal detachment (RD) is one of the major ocular diseases in Shih-Tzus. 1,2 Acquired RD in dogs is classified into two types in terms of pathophysiology, and is divided into three detailed types. 3 Rhegmatogenous RD (RRD) is caused by tears in the neurosensory retina, allowing fluid to enter the potential subretinal space. 3,4 Nonrheumatogenous RD is divided into exudative RD, which is caused by choroidal inflammatory and vascular disease, and tractional RD, which occurs when bands composed of inflammatory and fibrotic tissue form within the vitreous and subsequently exert anterior traction force on the neurosensory retina. 3,4 The most common cause of RRD is cataract surgery in dogs, 1 especially when surgery is complicated by tearing of the posterior lens capsule, vitreous loss, retained lens fragments, or intraocular hemorrhage. 1,2 Dogs with excessive vitreous degeneration, mainly Shih-Tzu, Boston Terrier, Poodle, etc., are prime candidates for RRD. 1,5 In previous reports, a giant retinal tear occurred in conjunction with vitreous degeneration and liquefaction in Shih-Tzus. 6 We have often seen retinal degeneration in the fellow eye in Shih-Tzus with unilateral RRD at Rakuno Gakuen University Veterinary Teaching Animal Hospital. In this study, we investigated disease in the fellow eye, and considered the relationship to RRD. Ó 2010 American College of Veterinary Ophthalmologists

2 290 itoh ET AL. MATERIALS AND METHODS Animals The fellow eyes (49 eyes) of 49 Shih-Tzus (27 male and 22 female; 1 14 years old; median age: 6.8 years old) with unilateral idiopathic RRD diagnosed by funduscopy or ultrasonography at Rakuno Gakuen University Teaching Animal Hospital from 2002 to 2005 were assessed in this study. Ophthalmic examinations Ophthalmic examinations, including menace response, pupillary light reflex, applanation tonometry (Tono-Pen XL applanation tonometer; Medtronic Solan, Jacksonville, FL, USA), slit-lamp biomicroscopy (SL-D7; Topcon, Tokyo, Japan), and funduscopy (TRC-50IX; Topcon, Tokyo, Japan) were carried out in all subjects. In 12 eyes, retinal degeneration was observed by funduscopy, and electroretingrams (ERGs) were recorded with a portable ERG LE-3000 (TOMEY, Aichi, Japan) and LED-electrode (H2000; Kyoto Contact Lens, Kyoto, Japan). ERG was performed under sedation by intravenous injection of a combination of 0.01 mg/kg medetomidine (Domitor; Meiji, Tokyo, Japan), 0.15 mg/kg midazolam (Dormicam; Astellas, Tokyo, Japan), and mg/kg butorphanol (Stadol; Bristol-Meyers, Tokyo, Japan), according to our previous report. 7 The pupils were fully dilated with 0.5% tropicamide and 0.5% phenylephrine hydrochloride (Mydrin-P; Santen, Osaka, Japan) before ERG examination. Three ERG responses were recorded with flash intensity of cd/m 2 /s for rod ERG, and 3.0 cd/m 2 /s for other responses, standard combined ERG, and 30 Hz flicker ERG. Rod and standard combined ERG were recorded after 30 min of dark adaptation, and 30 Hz flicker ERG was performed after 10 min of light adaptation. Subjects ERG amplitudes were compared with our normal data, consisting of ERG data from 16 eyes of nine Shih-Tzus (six male and three female; 4 10 years old; median age: 7.0 years old), without evident ocular disease. These normal Shih-Tzus were age-matched to the subjects of this study for ERG (Mann Whitney U-test, P > 0.05). The lower limit of normal ERG was statistically set as the mean value )1.96 SD. Follow-up We could perform follow-up in 35 eyes, over a period of 2 42 months, during which ophthalmic examinations, except for ERG, were performed in the fellow eyes periodically. RESULTS Menace response was present in 48 eyes, and was absent in one eye because of a mature cataract. Pupillary light reflex was normal or diminished, and intraocular pressure was within the normal range in all eyes. Results of slit-lamp biomicroscopy and ultrasonography are shown in Table 1. Cataracts were observed in 26 eyes (53%; incipient: 24 eyes; Table 1. Results of slit-lamp biomicroscopy, ultrasonography, and funduscopy in fellow eyes of 49 Shih-Tzus with unilateral retinal detachment Slit-lamp biomicroscopy and ultrasonography Cataract 26 (53 %) Incipient cataract 24 Immature cataract 1 Mature cataract 1 Vitreous presentation in anterior chamber 8 (16 %) Vitreous opacity 32 (65 %) Funduscopy Retinal degeneration 35 (71 %) ARV 15 ARV + HT 14 ARV + AO 2 ARV + HT + AO 4 ARV, attenuated retinal vessels; HT, hyper-reflectivity of tapetal fundus; AO, atrophy of optic disk. immature: 1 eye; mature: 1 eye). Vitreous presentation in the anterior chamber and opacities were seen in 8 (16%) and 32 eyes (65%), respectively. In funduscopy, retinal degeneration with various degrees of attenuated retinal vessels (ARV), hyper-reflectivity in the tapetal fundus (HR), and/or optic disk atrophy (OA) was observed in 35 eyes (71%; ARV only: 15 eyes; ARV and HR: 14 eyes; ARV and OA: 2 eyes, ARV, HR and OA: 4 eyes). Data of ERGs from 12 eyes are presented in Table 2. The amplitudes of rod, standard combined, and 30 Hz flicker ERG were decreased or nonrecordable in 5 (42%), 10 (83%), and 6 (50%) eyes, respectively, compared with agematched control data in Shi-Tzus (Table 2). Fundus photographs and ERGs of three cases, case 2, 7, and 8, are shown in Figs 1 3. During follow-up of 35 Shih-Tzus, RRD of the second eye occurred in six eyes (17%). In these six eyes, retinal degeneration and vitreous opacity had been detected in six (100%) and five eyes (83%), respectively. The time period between RRD of the first and second eye in these six cases was 2, 4, 6, 12, 15, and 30 months. These subjects included case 8, 10, and 11 in Table 2, and the period of RRD of the second eye was 30, 12, and 15 months, respectively. DISCUSSION In this study, we investigated factors in RRD in 49 Shih- Tzus with unilateral RRD. Ophthalmic examinations showed retinal degeneration and vitreous degeneration of various degrees in 71% and 65% of subjects, respectively. During the follow-up period, 17% of subjects showed RRD. From these results, we assume that retinal degeneration is also one of the factors in RRD in the Shih-Tzu, as for vitreous degeneration. The causes of retinal degeneration include genetic factors, developmental abnormalities, and intraocular inflammation. 3,8 16 However, there is no evidence that retinal degeneration itself causes RRD in dogs. In humans, a kind of

b-wave 1* 4 Female 53.25 47.75 100.00 30.75 2* 5 Male 70.75 87.75 122.50 34.25 3 5 Female 90.25 157.25 338.00 96.75 4 7 Male 65.50 98.75 177.25 47.00 5* 9 Male Non-rec. 33.00 45.00 18.

3 unilateral retinal detachment in shih-tzu 291 Table 2. Amplitudes of ERGs recorded from 12 eyes of Shih-Tzus with retinal degeneration and 16 eyes of normal control Shih-Tzus Case number Age (years) Sex ERG amplitude (lv) Rod Standard combined a-wave b-wave 1* 4 Female * 5 Male Female Male * 9 Male Non-rec * 10 Male * 10 Male * 10 Female * 10 Female Non-rec * 11 Female Non-rec * 11 Female Non-rec * 12 Female Normal control (mean) SD Lower limit *The case has a significant abnormal value, compared with normal control data. Median. Lower limit of normal = mean value ) 1.96 SD. ERG, electroretingram; non-rec., nonrecordable ERG; SD, standard deviation. 30 Hz flicker Figure 1. Fundus photograph and ERGs in 5-year-old male, case 2. Upper photograph is right fundus. Attenuation of retinal vessels, hyper-reflectivity in the tapetal fundus, optic disk atrophy, and vitreous opacity are observed. Lower photograph is left fundus with rhegmatogenous retinal detachment. ERGs recorded from right eye are shown; rod ERG, standard combined ERG, and 30 Hz flicker ERG from top to bottom, respectively. ERG, electroretinogram. Figure 2. Fundus photograph and ERGs in 10-year-old male, case 7. Upper photograph shows right fundus with rhegmatogenous retinal detachment. Lower photograph shows left fundus. Attenuation of retinal vessels and vitreous opacity are observed. ERGs recorded from the left eye are shown; rod ERG, standard combined ERG, and 30 Hz flicker ERG from top to bottom, respectively. retinal degeneration is the cause of RRD. 17 Thinning of degenerated retina and vitreous degeneration adjacent to retinal degeneration are factors in vitreoretinal traction and retinal tear. It is known that thinning of the retina is caused by retinal degeneration in dogs, 18,19 but secondary vitreous degeneration has not been reported. Thus, we presume that retinal degeneration in the Shih-Tzu may cause vitreous degeneration, as in humans, and would be one of the factors in RRD. Vitreous degeneration includes asteroid hyalosis, synchysis scintillans, and vitreous syneresis. These types of vitreous degeneration are caused by destabilization of the vitreous

292 itoh ET AL. Figure 3. Fundus photograph and ERGs in 10-year-old female, case 8. Upper photograph shows right fundus with rhegmatogenous retinal detachment. Lower photograph shows left fundus.

ERGs recorded from left eye are shown; rod ERG, standard combined ERG, and 30 Hz flicker ERG from top to bottom, respectively.

4 292 itoh ET AL. Figure 3. Fundus photograph and ERGs in 10-year-old female, case 8. Upper photograph shows right fundus with rhegmatogenous retinal detachment. Lower photograph shows left fundus. Attenuation of retinal vessels, hyper-reflectivity in tapetal fundus, optic disk atrophy and vitreous opacity are observed. ERGs recorded from left eye are shown; rod ERG, standard combined ERG, and 30 Hz flicker ERG from top to bottom, respectively. gel structure and vitreous liquefaction, and are one of the factors in RRD through loss of the function for retinal attachment. 2 Certain breeds, the Shih-Tzu, Boston terrier, and poodle, have a pre-disposition to vitreous degeneration and this often leads to RRD. 1,5 In our subjects, vitreous degeneration was frequently observed. No subject showed a hyper-mature cataract, although vitreous degeneration is common in eyes with a hyper-mature cataract. 20 These cataracts may be induced by progressive retinal atrophy, which is known as canine inherited retinopathy, and this causes secondary cataract through the release of toxic substances from the degenerative retina. 3,21 In humans, the relation between vitreous degeneration and RRD remains to be analyzed in detail. Foss and Wheeler 22 reported a strong correlation between vitreous liquefaction and posterior vitreous detachment. Focal posterior vitreous detachment rapidly develops into total vitreous detachment, and traction is exerted at the area of vitreoretinal adherence, separating the posterior vitreous cortex from the retina, with the development of a retinal tear and RRD It is known that vitreous gel movement secondary to eye movement exerts strong traction on all areas of vitreoretinal adherence, with excessive vitreoretinal traction and RRD development and enlargement. In dogs, there are no reports about vitreous degeneration secondary to retinal degeneration, and the relation between posterior vitreous detachment and RRD. However, if the same phenomenon were to occur, it is consistent that dogs with vitreous degeneration would be candidates for RRD. Reports in human 17,25 27 and rabbit 28 also support our hypothesis that retinal degeneration is one of the factors in RRD. Some reports show the utility of posterior vitrectomy in dogs. 6,29 Vainisi reported that 72% of their cases of RRD recovered after surgery. 5,6 However, the effects of surgery have not been confirmed, and the indications, complications, and durations for the surgery are unclear. There is no accepted preventive treatment of retinal degeneration. Prophylactic laser retinopexy has been performed recently as preventive treatment of RRD. 6,30 If the risk of RRD is increased by retinal degeneration, we propose that prophylactic laser retinopexy should be performed in cases of retinal degeneration and unilateral RRD, as RRD is difficult to cure, once it develops. In summary, retinal degeneration was frequently detected in the fellow eye of RRD by funduscopy and ERGs in Shih- Tzus. Retinal degeneration generally occurs bilaterally, so we consider that retinal degeneration was also present in the RD eye. In humans, it is reported that peripheral retinal degeneration is one of the causes of RRD. We suspect that retinal degeneration may be one of the causes of RRD also in Shih-Tzus. REFERENCES 1. Vainisi SJ, Wolfer JC. Canine retinal surgery. Veterinary Ophthalmology 2004; 7: Vainisi SJ, Wolfer JC, Smith PJ. Surgery of the Canine Posterior Segment. In: Veterinary Ophthalmology, 4th edn. (ed. Gelatt KN) Blackwell Publishing, Ames, 2007; Narfström K, Petersen-Jones S. Disease of Canine Ocular Fundus. In: Veterinary Ophthalmology, 4th edn. (ed. Gelatt KN) Blackwell Publishing, Ames, 2007; Rice TA, Wilkinson CP. Michels Retinal Detachment, 2nd edn. Mosby, St. Louis, Vainisi SJ. Retinal detachments. In: Small Animal Ophthalmology Secrets. (ed. Riis RC) Hanley and Belfus, Philadelphia, 2002; Vainisi SJ, Packo KH. Management of giant retinal tears in dogs. Journal of the American Veterinary Medical Association 1995; 206: Maehara S, Itoh N, Itoh Y et al. Electroretinography using contact lens electrode with built-in light source in dogs. Journal of Veterinary Medical Science 2005; 67: Bedford P. Collie eye anomaly in the Lancashire heeler. Veterinary Record 1998; 143: Gelatt KN, McGill LD. Clinical characteristics of microphthalmia with colobomas of the Australian Shepherd Dog. Journal of the American Veterinary Medical Association 1973; 162: Lahav M, Albert DM, Wyand S. Clinical and histopathologic classification of retinal dysplasia. American Journal of Ophthalmology 1973; 75: Appel M, Bistner SI, Manegus M. Pathogenicity of low virulent strains of two canine adenovirus types. American Journal of Veterinary Research 1973; 34:

5 unilateral retinal detachment in shih-tzu Acland G, Fletcher RT, Gentleman S et al. Non-allelism of three genes (rcd1, rcd2 and erd) for early-onset hereditary retinal degeneration. Experimental Eye Research 1989; 49: Aguirre G, Acland G. Variation in retinal degeneration phenotype inherited at the prcd locus. Experimental Eye Research 1988; 46: Albert RA. Lesions of the ocular fundus associated with systemic disease. Journal of the American Veterinary Medical Association 1970; 157: Stiles J. Canine rickettsial infections. The Veterinary Clinics of North America. Small Animal Practice 2000; 30: Hamernik KL. Proposed protocols for the determination of potential ocular effects of organophosphorus. Journal of Applied Toxicology 1994; 14: Byer NE. Lattice degeneration of the retina. Survey of Ophthalmology 1979; 23: Panzan CQ, Güven D, Weiland JD et al. Retinal thickness in normal and RCD1 dogs using optical coherence tomography. Ophthalmic Surgery Lasers and Imaging 2004; 35: Schmidt SY, Aguirre GD. Reductions in taurine secondary to photoreceptor loss in Irish setters with rod-cone dysplasia. Investigative Ophthalmology and Visual Science 1985; 26: Van der Woerdt A, Wilkie DH, Myer W. Ultrasonographic abnormalities in eyes of dogs with cataract: 147 cases ( ). Journal of the American Veterinary Medical Association 1993; 203: Gaiddon J, Lallement P, Peiffer R. Positive correlation between coat color and electroretinographically diagnosed progressive retinal atrophy in miniature poodles in Southern France. Veterinary and Comparative Ophthalmology 1995; 5: Foos RY, Wheeler NC. Vitreoretinal juncture. Synchysis senilis and posterior vitreous detachment. Ophthalmology 1982; 89: Machemer R. The importance of fluid absorption, traction, intraocular currents, and chorioretinal scars in the therapy of rhegmatogenous retinal detachments. American Journal of Ophthalmology 1974; 96: Sebag J. The Vitreous: Structure, Function and Pathology. Springer- Verlag, New York, Lewis H. Peripheral retinal degenerations and the risk of retinal detachment. American Journal of Ophthalmology 2003; 136: Sasaki K, Ideta H, Yonemoto J et al. Epidemiologic characteristics of rhegmatogenous retinal detachment in Kumamoto, Japan. Graefes Archive for Clinical and Experimental Ophthalmology 1995; 233: Pierro L, Camesasca FI, Mischi M et al. Peripheral retinal changes and axial myopia. Retina 1992; 12: Faude F, Francke M, Makarov F et al. Experimental retinal detachment causes widespread and multilayered degeneration in rabbit retina. Journal of Neurocytology 2001; 30: Grahn BH, Barnes LD, Breaux CB et al. Chronic retinal detachment and giant retinal tears in 34 dogs: outcome comparison of no treatment, topical medical therapy, and retinal reattachment after vitrectomy. Canadian Veterinary Journal 2007; 48: Pizzirani S, Davidson MG, Gilger BC. Transpupillary diode laser retinopexy in dogs: ophthalmoscopic, fluorescein angiographic and histopathologic study. Veterinary Ophthalmology 2003; 6:

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