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
069-8501, Japan
Address communications to:
S. Maehara
Tel.: +81 11-388-4853
Fax: +81 11-386-0880
e-mail: seiya-m@rakuno.ac.jp
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
reex, 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-reectivity 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 icker 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 classied 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 uid to enter the
potential subretinal space.
3,4
Nonrheumatogenous RD is
divided into exudative RD, which is caused by choroidal
inammatory and vascular disease, and tractional RD, which
occurs when bands composed of inammatory and brotic
tissue form within the vitreous and subsequently exert ante-
rior 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 frag-
ments, 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 vit-
reous 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 Uni-
versity Veterinary Teaching Animal Hospital. In this study,
we investigated disease in the fellow eye, and considered the
relationship to RRD.
2010 American College of Veterinary Ophthalmologists
Veterinary Ophthalmology (2010) 13, 5, 289293
MATERIALS AND METHODS
Animals
The fellow eyes (49 eyes) of 49 Shih-Tzus (27 male and 22
female; 114 years old; median age: 6.8 years old) with uni-
lateral idiopathic RRD diagnosed by funduscopy or ultraso-
nography 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 reex, 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 electroretin-
grams (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 0.025 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 ash intensity of 0.0096 cd/m
2
/s for rod
ERG, and 3.0 cd/m
2
/s for other responses, standard com-
bined ERG, and 30 Hz icker ERG. Rod and standard com-
bined ERG were recorded after 30 min of dark adaptation,
and 30 Hz icker 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; 410 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 (MannWhitney 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
242 months, during which ophthalmic examinations,
except for ERG, were performed in the fellow eyes peri-
odically.
RESULTS
Menace response was present in 48 eyes, and was absent in
one eye because of a mature cataract. Pupillary light reex
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;
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 degener-
ation with various degrees of attenuated retinal vessels
(ARV), hyper-reectivity 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 icker
ERG were decreased or nonrecordable in 5 (42%), 10
(83%), and 6 (50%) eyes, respectively, compared with age-
matched control data in Shi-Tzus (Table 2). Fundus photo-
graphs and ERGs of three cases, case 2, 7, and 8, are shown
in Figs 13.
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 ve eyes (83%), respectively. The time period
between RRD of the rst 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 vitre-
ous degeneration.
The causes of retinal degeneration include genetic factors,
developmental abnormalities, and intraocular inamma-
tion.
3,816
However, there is no evidence that retinal degen-
eration itself causes RRD in dogs. In humans, a kind of
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-reectivity of tapetal
fundus; AO, atrophy of optic disk.
290 i + on E T A L .
2010 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 13, 289293
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, synchy-
sis scintillans, and vitreous syneresis. These types of vitreous
degeneration are caused by destabilization of the vitreous
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
30 Hz
icker a-Wave 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 18.00
6* 10 Male 80.50 114.38 126.31 51.25
7* 10 Male 24.25 56.25 74.50 32.75
8* 10 Female 40.00 87.00 79.75 48.30
9* 10 Female Non-rec. 19.00 56.75 10.00
10* 11 Female Non-rec. 44.67 58.83 37.50
11* 11 Female Non-rec. 110.92 126.50 58.00
12* 12 Female 50.50 43.75 113.00 44.75
Normal control (mean) 7.0 112.68 118.14 221.27 70.86
SD 2.1 37.53 30.26 44.55 16.13
Lower limit 39.13 58.82 133.95 39.26
*The case has a signicant 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.
Figure 1. Fundus photograph and ERGs in
5-year-old male, case 2. Upper photograph is right
fundus. Attenuation of retinal vessels, hyper-reec-
tivity in the tapetal fundus, optic disk atrophy, and
vitreous opacity are observed. Lower photograph is
left fundus with rhegmatogenous retinal detach-
ment. ERGs recorded from right eye are shown; rod
ERG, standard combined ERG, and 30 Hz icker
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 icker ERG from top to bottom,
respectively.
txi r a + r r a r r r + i xa r rr + a c nr x+ i x s ni n- + z t 291
2010 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 13, 289293
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 cata-
racts 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 ana-
lyzed in detail. Foss and Wheeler
22
reported a strong corre-
lation 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 develop-
ment of a retinal tear and RRD.
2224
It is known that vitre-
ous gel movement secondary to eye movement exerts strong
traction on all areas of vitreoretinal adherence, with exces-
sive 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 con-
sistent that dogs with vitreous degeneration would be candi-
dates for RRD. Reports in human
17,2527
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 conrmed, and the indications, complica-
tions, and durations for the surgery are unclear. There is no
accepted preventive treatment of retinal degeneration. Pro-
phylactic 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 prophy-
lactic laser retinopexy should be performed in cases of reti-
nal degeneration and unilateral RRD, as RRD is difcult 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.
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