J. COMP.
PATH.
1975. VOL.
85.
195
RHEGJJATOGENOUS
BILATERAL
DETACHMENT
IN
A POODLE
RETINAL DOG
BY
E. H. Instiiute for General Pathology
and Pathological
SCHAFFER
Anatomy, Faculty F.R.G.
of Veterinary
Medicine,
Uniuersily
of Munich,
and I.
H.
University
L.
WALLOW
Eye Hospital,
Munich,
F.R.G.
INTRODUCTION
In the study of naturally occurring diseases in animals retinal detachment in dogs has been used to obtain an insight into similar conditions in man (Okun, Rubin and Collins, 1961). Retinal detachment in dogs is rare and is restricted to the Scotch (rough) Collie and to the Sheltie (Shetland Sheep Dog). In these species it is associated with congenital posterior staphylomas (Donovan and Wyman, 1965; Donovan, Mackenzie, Freeman and Schepens, 1969; Blogg, 1970; Mason and Cox, 1971). It has been assumed that, in general, the canine vitreous seems to undergo no typical posterior detachment, so that horseshoeshaped or operculated retinal tears that give rise to retinal detachment do not develop (Okun et al., 1961). Recently we observed a retinal detachment in a middle-aged poodle, which was bilateral, and showed operculated tears associated with adherent vitreous strands. The histopathological features of this case form the present study. MATERIALS
AND
METHODS
A 7-year-old black and tan male poodle dog was presented at the Department of Surgery, University of Munich, for ocular examination after having suffered loss of vision. No signs of accidental ocular trauma had been noticed previously. Ophthalmoscopic examination revealed bilateral retinal detachment. The dog belonged to a breed in which retinal detachment had never been noted before. Treatment was not attempted because of the poor prognosis and the dog was destroyed at the owner’s request. Both eyes were enucleated and fixed in 10 per cent. neutral buffered formalin, and sections, grossly examined under a dissecting microscope, were photographed. They were then embedded in Bioloid@, cut at 5 pm. either serially or in step sections and stained with HE and PAS. RESULTS
Macroscopic Findings The fixed globes measured 21 x 20 x 20 mm. in their antero-posterior, horizontal and vertical diameters. Both corneas measured 13 x 13 mm. in their horizontal and vertical meridians, respectively. There was a total retinal
196
Fig.
E. H. SCHiFFER
AND
1. Gross section of left eye. Extensive detachment equatorial giant hole. Multiple confluent smaller hole (arrows) (CP=ciliary process) x Z-5.
I. H.
L. WALLOW
of the retina (R) in combination tears can be seen at the peripheral
with an area of ‘the
Fig. 2. The central region of the posterior segment of the right globe. The detached retina (R) is projected into the vitreous (V) and fixed only at the optic nerve head. The outer plexiform layer ofthe retina shows cystoid degeneration. At the peripheral ends of the hole the retina is thickened and curled inwards. (The liquified vitreous body has been removed and the space therefore appears empty). PAS x 12.
CANINE
RHEGMATOGENOUS
RETINAL
DETACHMENT
Fig. 3. The peripheral area of the hole. (a) At the edge of the hole the detached retina (R) is thickened and gliotic and the architecture of the different layers is loosened by cystoid degeneration. At the ora (0) the thinned retina blends with the unpigmented epithelium of the ciliary body. PAS x 24. (b) (Detail of the detached retina at the edge of the hole from Fig. 3a). Condensed vitreous strands (V) adhere to the surface of the retina which shows marked gliosis. Numerous pigment-laden macrophages (M) are interspersed within the retina and the cortical vitreous. PAS x 76. (c) (Detail of the retina distant to the hole area from Fig. 3a). The detachment continues anteriorly beyond the ora by a detachment of the unpigmented epithelium (UEP) of the pars plana from the pigmented epithelium (PEP) of the pars plana. PAS x 76.
198
E. H. SCHAFFER
AND
I. H. L. WALLOW
Fig. 4. The central area of the hole. (a) The detached and degenerated retina (R) is curled inwards and shows irregularities of its architecture. PAS x 76. (b) (Details of the vicinity of the central area of the hole). The thinned retina (R) is adherent partly to the retinal pigmented epithelial cells (RPE), partly to Bruch’s membrane (BM). PAS x 76. (c) So-called retinal puckering in central parts of the retina (R) caused by adherent vitreous strands (V). PAS x 76. (d) (Detail of the central area of the hole). Button-shaped irregularities of the retinal pigmented epithelial cells (RPE) in the detachment zone. PAS x 76.
CANINE
RHEGMATOGENOUS
RETINAL
199
DETACHMENT
detachment of the right eye showing also liquified vitreous. Under the dissecting microscope, some remaining pillars of a giant and almost circular peripheral retinal tear were identified. The left eye revealed an extensive retinal detachment associated with a peripheral break and multiple confluent smaller tears (Fig. 1). The central part of the detached retina of this eye was retracted and rolled inwards. The posterior segments of both eyes were apparently normal. Microscopic Findings The large extension of the almost circular retinal tear in the right eye, allowing the formation of deep retinal folds, is illustrated in Fig. 2. Subsequent figures present details of the retinal periphery of the left eye from areas indicated by arrows in Fig. 1. The retina near the peripheral edge of the giant tear was widely separated from the retinal pigment epithelium; it was thinned and showed cystoid degeneration (Fig. 3a). The peripheral edge of the giant tear was rounded and there was marked gliosis of the retina in this area. Many pigment-laden macrophages were interspersed within the retina and within the cortical vitreous. Dense vitreous strands adhered to the inner retinal aspect
Fig. 5. Detached, round and gliotic vicinity of a hole area. PAS
x
retinal 120.
operculum
adherent
to condensed
vitreous
strands
in the
(Fig. 3b). More peripherally, there was separation of the epithelium of the pars plana (Fig. 3~). The retina near the central edge of the giant tear had a tendency to curl inwards and there was a wide range of retinal degeneration. In some areas, only cystoid spaces were present; in others, the outer retinal half was diffusely atrophic (Fig. 4a). Focally, the retina was thinned to a few layers of cellular membrane intimately adherent to the retinal pigment epithelium or to Bruch’s membrane (Fig. 4b). Smaller vitreous strands near this region were associated with fixed atrophic retinal folds (“retinal puckering”) (Fig. 4~). The retinal pigment epithelial cells in the area of the retinal detachment showed button-shaped irregularities (Fig. 4d). Multiple operculated retinal holes were observed in the vicinity of the giant tear (Fig. 5).
200
E. H.
SCHIiFFER
AND
I. H.
L. WALLOW
DISCUSSION
Although it is thought that retinal detachment in man has profound differences compared with the dog, in this case of a bilateral retinal detachment in a poodle there were numerous features that were similar to the situation in primates or in man. A bilateral peripheral flap type and giant holes were observed as well as operculated tears associated with complete retinal detachment in combination with liquified vitreous such as is seen in man (Hogan and Zimmerman, 1968). The degenerative changes in the retina which were seen as peripheral cystoid degeneration and thinning of the outer layers of the neural retina were identical to the findings in man. Hogan and Zimmerman (1968) discussing the pathogenesis in man state that, if trauma, inflammation, haemorrhage and systemic diseases are eliminated, there remain a large number ofdetachments which are due to some obscure retinal or vitreo-retinal degeneration. One of these changes in man is the peripheral cystoid degeneration. The reason for the development of these so-called presenile degenerative lesions in the retina is not known, but because of their frequency and because they principally affect certain portions of the retina, it is believed that some defect in nutrition or blood supply plays a part (Hogan and Zimmerman, 1968). Cystic degeneration of the peripheral retina and retinal breaks in these areas are also a common finding in theseniledogeye (Everett, 1957; Okun, &al., 1961). However, the prevalence of “idiopathic” retinal detachment, as stated by Okun et al. (1961), appears to be more rare in the dog than in man, ifit occurs at all. These authors therefore, conclude that these breaks rarely, if ever, lead to retinal detachment in the dog. Okun et al. (1961) claimed that the reason for the dog’s eye remaining immune to “idiopathic” retinal detachment could be most likely explained by the absence of posterior vitreous detachment, a finding which is in contrast to the situation in man and in this case in which we found typical flap type and operculated holes in association with typical posterior vitreous detachment. The important role of vitreous as a causative factor in retinal detachment is thus demonstrated for the dog’s eye. In addition, we observed features which have been noted in experimental retinal detachment in the owl monkey (Machemer, 1968) and in retinal repair after xenon arc photocoagulation in the rhesus monkey (Wallow and TSO, 1973a,b). Thus the retinal epithelial cells in the area of the retinal detachment showed buttonshaped irregularities ; in other areas there were foci of spontaneous retinal reattachment with adhesions between the thinned retina to either the retinal pigment epithelium or to Bruch’s membrane. No similar observations have been reported in the poodle. Recalling the different type of retinal detachment in Collies and Shelties one may speculate that differences between different breeds of dogs may be found which allow inclusion of a type that is susceptible to the form of retinal detachment most common in man. Some dogs may, therefore, be useful for the study of certain ocular diseases in man (Okun et al., 1961).
CANINE
RHEGMATOGENOUS
RETINAL
201
DETACHMENT
SUMMARY
A 7-year-old male poodle dog which had suffered loss of vision was destroyed. On macroscopical and histopathological examination both eyes revealed an extensive retinal detachment associated with typical flap type and operculated holes in combination with typical posterior vitreous detachment. In the area of the holes the retina was widely separated from the retinal pigment epithelium and it was thinned showing cystoid degeneration. In man, these changes which are characteristic of certain types of rhegmatogenous retinal detachments may be assumed for the case in the poodle dog. ACKSOWLEDGMENTS
Mrs Barbara
Schmitz is thanked for preparing
the histological
material.
REFERENCES
Blogg, R. J. (1970). Collie eye anomaly. Australian Veterinary Journal, 46, 530-532. Donovan, E. F., and Wyman, M. ( 1965). 0 cu1ar fundus anomaly in the collie. Journal of the American Veterinary Medical Association, 147, 1465-I 469. Donovan, R. H., Mackenzie Freeman, H., and Schepens,Ch. L. (1969). Anomaly of the collie eye. Journal of the American Veterinary Medical Association, U&%72-%7%. Everett, W. G. (1957). Peripheral cystic degeneration of the retina: A preliminary report. American Journal of Ophthalmology, 43, 472. Hogan, M. J., and Zimmerman, L. E. (196%). Retinal detachment. In Ophthalmic Pathology, an Atlas and Textbook, 3rd edit., pp. 549-570, W. B. Saunders Company, Philadelphia and London. Machemar, R. (196%). Experimental retinal detachment in the owl monkey II Histology of retina and pigment epithelium. American Journal of Ophthalmology. 66, 396-410. Mason, T. A., and Cox, K. (1971). Collie eye anomaly. Australian Veterinary Journal, 47, 38-40. Okun, E., Rubin, L. F., and Collins, E. M. (1961). Retinal breaks in the senile dog eye. Archives of OphthalmoloQ, 66, 702-707. Roberts, S. R. (1969). The collie eye anomaly. Journal of the American Veterinary Medical
Association,
155, 859-866.
Wallow, I. H. L., and Tso, M. 0. M. (1973a). Repair after xenon arc photocoagulation. 2. A clinical and light microscopic study on the evolution of retinal lesionsin the rhesus monkey. American Journal of Ophthalmology, 75, 610-626. Wallow, I. H. L., and Tso, M. 0. M. (1973b). Repair after xenon arc photocoagulation. 3. The evolution of retinal lesionsin the rhesusmonkey. An electron microscopic study. American Journal of Ophthalmology, 75, 957-972. [Received
for
publication,
June 12th, 19741
PATH.
1975. VOL.
85.
195
RHEGJJATOGENOUS
BILATERAL
DETACHMENT
IN
A POODLE
RETINAL DOG
BY
E. H. Instiiute for General Pathology
and Pathological
SCHAFFER
Anatomy, Faculty F.R.G.
of Veterinary
Medicine,
Uniuersily
of Munich,
and I.
H.
University
L.
WALLOW
Eye Hospital,
Munich,
F.R.G.
INTRODUCTION
In the study of naturally occurring diseases in animals retinal detachment in dogs has been used to obtain an insight into similar conditions in man (Okun, Rubin and Collins, 1961). Retinal detachment in dogs is rare and is restricted to the Scotch (rough) Collie and to the Sheltie (Shetland Sheep Dog). In these species it is associated with congenital posterior staphylomas (Donovan and Wyman, 1965; Donovan, Mackenzie, Freeman and Schepens, 1969; Blogg, 1970; Mason and Cox, 1971). It has been assumed that, in general, the canine vitreous seems to undergo no typical posterior detachment, so that horseshoeshaped or operculated retinal tears that give rise to retinal detachment do not develop (Okun et al., 1961). Recently we observed a retinal detachment in a middle-aged poodle, which was bilateral, and showed operculated tears associated with adherent vitreous strands. The histopathological features of this case form the present study. MATERIALS
AND
METHODS
A 7-year-old black and tan male poodle dog was presented at the Department of Surgery, University of Munich, for ocular examination after having suffered loss of vision. No signs of accidental ocular trauma had been noticed previously. Ophthalmoscopic examination revealed bilateral retinal detachment. The dog belonged to a breed in which retinal detachment had never been noted before. Treatment was not attempted because of the poor prognosis and the dog was destroyed at the owner’s request. Both eyes were enucleated and fixed in 10 per cent. neutral buffered formalin, and sections, grossly examined under a dissecting microscope, were photographed. They were then embedded in Bioloid@, cut at 5 pm. either serially or in step sections and stained with HE and PAS. RESULTS
Macroscopic Findings The fixed globes measured 21 x 20 x 20 mm. in their antero-posterior, horizontal and vertical diameters. Both corneas measured 13 x 13 mm. in their horizontal and vertical meridians, respectively. There was a total retinal
196
Fig.
E. H. SCHiFFER
AND
1. Gross section of left eye. Extensive detachment equatorial giant hole. Multiple confluent smaller hole (arrows) (CP=ciliary process) x Z-5.
I. H.
L. WALLOW
of the retina (R) in combination tears can be seen at the peripheral
with an area of ‘the
Fig. 2. The central region of the posterior segment of the right globe. The detached retina (R) is projected into the vitreous (V) and fixed only at the optic nerve head. The outer plexiform layer ofthe retina shows cystoid degeneration. At the peripheral ends of the hole the retina is thickened and curled inwards. (The liquified vitreous body has been removed and the space therefore appears empty). PAS x 12.
CANINE
RHEGMATOGENOUS
RETINAL
DETACHMENT
Fig. 3. The peripheral area of the hole. (a) At the edge of the hole the detached retina (R) is thickened and gliotic and the architecture of the different layers is loosened by cystoid degeneration. At the ora (0) the thinned retina blends with the unpigmented epithelium of the ciliary body. PAS x 24. (b) (Detail of the detached retina at the edge of the hole from Fig. 3a). Condensed vitreous strands (V) adhere to the surface of the retina which shows marked gliosis. Numerous pigment-laden macrophages (M) are interspersed within the retina and the cortical vitreous. PAS x 76. (c) (Detail of the retina distant to the hole area from Fig. 3a). The detachment continues anteriorly beyond the ora by a detachment of the unpigmented epithelium (UEP) of the pars plana from the pigmented epithelium (PEP) of the pars plana. PAS x 76.
198
E. H. SCHAFFER
AND
I. H. L. WALLOW
Fig. 4. The central area of the hole. (a) The detached and degenerated retina (R) is curled inwards and shows irregularities of its architecture. PAS x 76. (b) (Details of the vicinity of the central area of the hole). The thinned retina (R) is adherent partly to the retinal pigmented epithelial cells (RPE), partly to Bruch’s membrane (BM). PAS x 76. (c) So-called retinal puckering in central parts of the retina (R) caused by adherent vitreous strands (V). PAS x 76. (d) (Detail of the central area of the hole). Button-shaped irregularities of the retinal pigmented epithelial cells (RPE) in the detachment zone. PAS x 76.
CANINE
RHEGMATOGENOUS
RETINAL
199
DETACHMENT
detachment of the right eye showing also liquified vitreous. Under the dissecting microscope, some remaining pillars of a giant and almost circular peripheral retinal tear were identified. The left eye revealed an extensive retinal detachment associated with a peripheral break and multiple confluent smaller tears (Fig. 1). The central part of the detached retina of this eye was retracted and rolled inwards. The posterior segments of both eyes were apparently normal. Microscopic Findings The large extension of the almost circular retinal tear in the right eye, allowing the formation of deep retinal folds, is illustrated in Fig. 2. Subsequent figures present details of the retinal periphery of the left eye from areas indicated by arrows in Fig. 1. The retina near the peripheral edge of the giant tear was widely separated from the retinal pigment epithelium; it was thinned and showed cystoid degeneration (Fig. 3a). The peripheral edge of the giant tear was rounded and there was marked gliosis of the retina in this area. Many pigment-laden macrophages were interspersed within the retina and within the cortical vitreous. Dense vitreous strands adhered to the inner retinal aspect
Fig. 5. Detached, round and gliotic vicinity of a hole area. PAS
x
retinal 120.
operculum
adherent
to condensed
vitreous
strands
in the
(Fig. 3b). More peripherally, there was separation of the epithelium of the pars plana (Fig. 3~). The retina near the central edge of the giant tear had a tendency to curl inwards and there was a wide range of retinal degeneration. In some areas, only cystoid spaces were present; in others, the outer retinal half was diffusely atrophic (Fig. 4a). Focally, the retina was thinned to a few layers of cellular membrane intimately adherent to the retinal pigment epithelium or to Bruch’s membrane (Fig. 4b). Smaller vitreous strands near this region were associated with fixed atrophic retinal folds (“retinal puckering”) (Fig. 4~). The retinal pigment epithelial cells in the area of the retinal detachment showed button-shaped irregularities (Fig. 4d). Multiple operculated retinal holes were observed in the vicinity of the giant tear (Fig. 5).
200
E. H.
SCHIiFFER
AND
I. H.
L. WALLOW
DISCUSSION
Although it is thought that retinal detachment in man has profound differences compared with the dog, in this case of a bilateral retinal detachment in a poodle there were numerous features that were similar to the situation in primates or in man. A bilateral peripheral flap type and giant holes were observed as well as operculated tears associated with complete retinal detachment in combination with liquified vitreous such as is seen in man (Hogan and Zimmerman, 1968). The degenerative changes in the retina which were seen as peripheral cystoid degeneration and thinning of the outer layers of the neural retina were identical to the findings in man. Hogan and Zimmerman (1968) discussing the pathogenesis in man state that, if trauma, inflammation, haemorrhage and systemic diseases are eliminated, there remain a large number ofdetachments which are due to some obscure retinal or vitreo-retinal degeneration. One of these changes in man is the peripheral cystoid degeneration. The reason for the development of these so-called presenile degenerative lesions in the retina is not known, but because of their frequency and because they principally affect certain portions of the retina, it is believed that some defect in nutrition or blood supply plays a part (Hogan and Zimmerman, 1968). Cystic degeneration of the peripheral retina and retinal breaks in these areas are also a common finding in theseniledogeye (Everett, 1957; Okun, &al., 1961). However, the prevalence of “idiopathic” retinal detachment, as stated by Okun et al. (1961), appears to be more rare in the dog than in man, ifit occurs at all. These authors therefore, conclude that these breaks rarely, if ever, lead to retinal detachment in the dog. Okun et al. (1961) claimed that the reason for the dog’s eye remaining immune to “idiopathic” retinal detachment could be most likely explained by the absence of posterior vitreous detachment, a finding which is in contrast to the situation in man and in this case in which we found typical flap type and operculated holes in association with typical posterior vitreous detachment. The important role of vitreous as a causative factor in retinal detachment is thus demonstrated for the dog’s eye. In addition, we observed features which have been noted in experimental retinal detachment in the owl monkey (Machemer, 1968) and in retinal repair after xenon arc photocoagulation in the rhesus monkey (Wallow and TSO, 1973a,b). Thus the retinal epithelial cells in the area of the retinal detachment showed buttonshaped irregularities ; in other areas there were foci of spontaneous retinal reattachment with adhesions between the thinned retina to either the retinal pigment epithelium or to Bruch’s membrane. No similar observations have been reported in the poodle. Recalling the different type of retinal detachment in Collies and Shelties one may speculate that differences between different breeds of dogs may be found which allow inclusion of a type that is susceptible to the form of retinal detachment most common in man. Some dogs may, therefore, be useful for the study of certain ocular diseases in man (Okun et al., 1961).
CANINE
RHEGMATOGENOUS
RETINAL
201
DETACHMENT
SUMMARY
A 7-year-old male poodle dog which had suffered loss of vision was destroyed. On macroscopical and histopathological examination both eyes revealed an extensive retinal detachment associated with typical flap type and operculated holes in combination with typical posterior vitreous detachment. In the area of the holes the retina was widely separated from the retinal pigment epithelium and it was thinned showing cystoid degeneration. In man, these changes which are characteristic of certain types of rhegmatogenous retinal detachments may be assumed for the case in the poodle dog. ACKSOWLEDGMENTS
Mrs Barbara
Schmitz is thanked for preparing
the histological
material.
REFERENCES
Blogg, R. J. (1970). Collie eye anomaly. Australian Veterinary Journal, 46, 530-532. Donovan, E. F., and Wyman, M. ( 1965). 0 cu1ar fundus anomaly in the collie. Journal of the American Veterinary Medical Association, 147, 1465-I 469. Donovan, R. H., Mackenzie Freeman, H., and Schepens,Ch. L. (1969). Anomaly of the collie eye. Journal of the American Veterinary Medical Association, U&%72-%7%. Everett, W. G. (1957). Peripheral cystic degeneration of the retina: A preliminary report. American Journal of Ophthalmology, 43, 472. Hogan, M. J., and Zimmerman, L. E. (196%). Retinal detachment. In Ophthalmic Pathology, an Atlas and Textbook, 3rd edit., pp. 549-570, W. B. Saunders Company, Philadelphia and London. Machemar, R. (196%). Experimental retinal detachment in the owl monkey II Histology of retina and pigment epithelium. American Journal of Ophthalmology. 66, 396-410. Mason, T. A., and Cox, K. (1971). Collie eye anomaly. Australian Veterinary Journal, 47, 38-40. Okun, E., Rubin, L. F., and Collins, E. M. (1961). Retinal breaks in the senile dog eye. Archives of OphthalmoloQ, 66, 702-707. Roberts, S. R. (1969). The collie eye anomaly. Journal of the American Veterinary Medical
Association,
155, 859-866.
Wallow, I. H. L., and Tso, M. 0. M. (1973a). Repair after xenon arc photocoagulation. 2. A clinical and light microscopic study on the evolution of retinal lesionsin the rhesus monkey. American Journal of Ophthalmology, 75, 610-626. Wallow, I. H. L., and Tso, M. 0. M. (1973b). Repair after xenon arc photocoagulation. 3. The evolution of retinal lesionsin the rhesusmonkey. An electron microscopic study. American Journal of Ophthalmology, 75, 957-972. [Received
for
publication,
June 12th, 19741
