Senile disciform macular degeneration

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1 British Journal of Ophthalmology, 1977, 61, Senile disciform macular degeneration in the second eye Z. GREGOR, A. C. BIRD, AND I. H. CHISHOLM From Moorfields Eye Hospital and Institute of Ophthalmology, London SUMMARY Development of senile disciform degeneration in the second eye was studied in a group of 14 patients over a period of up to five years. 12 to 15% of these patients develop disciform degeneration in the other eye each year. Patients with large and confluent drusen, especially if combined with accumulation of dye on fluorescein angiogram, were at greatest risk of developing disciform degeneration in the second eye. Disciform macular degeneration is characterised by elevation of the pigment epithelium and retina by blood, serous fluid, and invasion of the subpigment epithelial space by fibrovascular tissue arising from the choroid. Drusen were first described by Donders (1885), but it was not until 194 that they were recognised as a predisposing cause of disciform detachment of the macula (Gifford and Cushman, 194). Subsequent experience has confirmed this association, so that now it is generally acknowledged that senile disciform macular degeneration occurs as a result of pre-existing changes in Bruch's membrane and the pigment epithelium. These changes may be the result of a genetically determined disorder (Gass, 1973) or of age alone, but the nature of the changes and the manner by which they induce the disciform response have yet to be identified precisely. With increasing age Bruch's membrane becomes thicker (Hogan, 1967; Hogan et al., 1971). Collagen fibres become electron dense, and irregularly banded structures appear which may be the result of degenerating collagen (Hogan et al., 1971). The elastic zone becomes basophilic, the elastic fibres increase in electron density, and needlelike crystals are deposited within the fibres. Accompanying the fibre changes there is deposition of PASpositive granular, vesicular, and filamentary material in the matrix of the inner collagen layer at first and later in the elastic zone. This material resembles the contents of pigment epithelial phagosomes, and the suggestion has been made that it consists of discharged phagosomal material (Hogan et al., 1971). It has also been inferred that drusen were formed by accumulation of this material between the inner Address for reprints: Dr A. C. Bird, Moorfields Eye Hospital, City Road, London EC1V 2PD collagen layer of Bruch's membrane and the pigment epithelial basement membrane. This material probably forms the linear deposits described by Sarks (1973) which form a patchy and then continuous layer on the inner surface of Bruch's membrane. If Bruch's membrane acts as a physical barrier to blood vessel growth, the degeneration of fibres and the distortion of fibres by accumulation of abnormal material within Bruch's membrane may allow vascular incursion into the subpigment epithelial space. Blood vessel growth may be stimulated by outer retinal ischaemia if the thickened membrane acts as a diffusion barrier. Furthermore, the presence of macrophages on the inner surface of Bruch's membrane, as described by Sarks (1976), may also stimulate blood vessel growth. It is also relevant that penetration of Bruch's membrane by choroid vessels is common in the eyes of the elderly, being multifocal and occurring throughout the fundus (Brown, 194; Riechling and Klemens, 194; Friedman et al., 1963), whereas recognisable disciform lesions are usually in the macular region and appear to arise from a single vascular source. From the clinical standpoint limited studies have been undertaken concerning the risk of visual loss of an eye with drusen (Teeters and Bird, 1973; Gass, 1973; Chandra et al., 1974). The exact prognostic significance of the type and number of drusen has not yet been defined, though Gass (1973) and Chandra and co-workers (1974) implied that a greater number of drusen denoted worse prognosis. Other poor prognostic signs have been suggested, including rapid increase in the number of drusen, extensive associated pigment epithelial changes, and disciform degeneration in the other eye (Gass, 1973). 141

2 142 Z. Gregor, A. C. Bird, and 1. H. Chisholm In the first part of this paper we record the incidence of second eye involvement in a group of patients with unilateral senile disciform macular degeneration who have been observed for periods varying between 1 and 5 years. In the second study reported a qualitative and quantitative assessment of predisposing changes was made, and an attempt was made to identify the type of change which put a patient at high risk of developing a lesion in the second eye. I. INCIDENCE Materials and methods 1-1' 4-75 C5 ff a All patients between the ages of 6 and 69 who presented initially to Moorfields Eye Hospital with visual loss due to senile disciform macular degeneration and were seen in the retinal diagnostic department from 197 until the end of 1974 were reviewed. A large number of patients referred from other hospitals and those over 69 were not included because of difficulties of follow-up. In our group there were 172 patients. Of these, 14 had a disciform lesion in one eye only at the time of presentation and had been followed up for at least one year. All patients with a disciform lesion had serous elevation of the retina and the pigment epithelium and subretinal blood vessels were recognised on fluorescein angiography. Results Twenty-nine patients developed a disciform lesion in the second eye during the period of follow-up. The results were analysed in two ways-in respect of length of follow-up and in respect of annual risk in completed years of observation. I. PATIENT RESULTS During the first year of follow-up 9 (9 8 %) of the 14 patients developed a disciform lesion in the other eye. Of these, 74 were followed up for 2 years, and 18 (19%) developed disciform degeneration in the fellow eye during this period. The figures for incidence of involvement of the second eye for those followed up for 3 years was 17 of 53 (3%), for 4 years was 11 of 23 (48 %), and for 5 years, 5 of 11 (45%) (Fig. 1). II. YEARLY RESULTS Of the 34 patients 5 (15%) followed up in 1972 developed a disciform lesion in the other eye. The incidence for 1973 was 6 of 49 patients (12%) and for 1974, 12 of 78 patients (15%) (Fig. 2). 4.s Q Ool 1 75.@ CX 5' iss--sd-y--- h.s:4 6: a - c Years of follow-up Fig. I Patient results. (a) Proportion ofpatients who developed a disciform lesion in the second eye over the period offollow-up (shaded section of column). (b) Same expressed as percentages. (c) Comparison with calculated incidence curve of 12 % per year Comments In respect of yearly incidence the risk of developing a disciform lesion in the second eye appears to lie between 12 and 15%. This is in agreement with the incidence of 12% found by Teeters and Bird (1973), and 35 % in 3 years by Gass (1973). The results in terms of patient follow-up suggest a constant risk of 12% per year of developing a second disciform lesion during the first 5 years. A second disciform lesion does not appear to be inevitable within any given period. It is unlikely that the risk in the 6 to 69 age group can be applied to younger patients. Equally the risk may not pertain to people witlh

3 Senile disciform macular degeneration in the second eye c *u z 5 Fig. 2. Yearly results. (a) Proportion of patients who developed a disciform lesion in the other eye each year (shaded section of column). Both drusen and pigment epithelial changes were examined on the initial colour stereophotographs. The following characteristics of drusen were assessed: Total number and distribution, whether macular or perimacular. Single dome-shaped drusen were arbitrarily divided into four categories according to their diameter: Less than 5,um; 5 to 15 l±m; 1 Z 7s.IV so.s a- (b) Same expressed as percentages bilateral drusen and pigment epithelial changes without disciform lesions. Gass (1973) has clearly shown the relatively lower risk of developing a disciform lesion in these two groups. In his series a smaller proportion of eyes in patients with no disciform lesions suffered visual loss than in those with unilateral disciform degeneration, and in the latter group the average age of patients suffering visual loss in the second eye was higher than in the original sample. II. SIGNIFICANCE OF PREDISCIFORM CHANGES IN THE SUBSEQUENT DEVELOPMENT OF SENILE DISCIFORM MACULAR DEGENERATION Materials and methods All 14 patients in the original sample had a full ophthalmological examination which included fundus colour stereophotography and fluorescein angiography. All the patients have had repeated examinations during the period of follow-up (29 of these 14 patients developed a disciform lesion in the other eye during this period). A Zeiss (Oberkochen) fundus camera was used to obtain both colour photographs and fluorescein angiograms. The initial colour photographs and fluorescein angiograms of the eye with predisciform changes were examined under magnification. The macular region was arbitrarily divided into sectors by placing a grid over the photograph (Figs. 3 and 4). Fig. 3 The measuring grid. Inner complete ring corresponds to a diameter of 16 tm (I DD), outer ring to 48 j±m (3 DD). The distances between the dividing marks correspond to 2 l±m in the inner ring and 4 Ftm in the outer ring Fig. 4 The measuring grid is placed on a standard fundus photograph, centred on the fovea. The size and distances offundus abnormalities can be assessed

4 144 2 to 5,um; 5 to 8 sum. Sheets of white subpigment epithelial material with an irregular surface were categorised as confluent. In respect of the edge of the drusen, they were separately recorded as having well-defined or blurred edges. The corresponding fluorescein angiograms were examined. The following features were noted: accumulation of dye, transmission defect or a normal appearance. All the findings were recorded on a standard form. Pigment epithelial changes were recognised either as pigment clumping on the surface of the drusen or without underlying drusen, and as pigment epithelial atrophy with or without coexisting choroidal atrophy. Although the following features were recorded, they were not used in the final analysis. The colour of drusen was difficult to assess because of variation in the quality of the original photographs or lens opacities or the likelihood of observer error. Drusen with white glistening surfaces, usually thought to denote calcification, were observed infrequently. In the presence of widespread drusen pigment epithelial atrophy without choroidal atrophy was also difficult to estimate. To minimise bias and to maintain standardisation, the following steps were adhered to: (1) The patient records were examined at random without prior knowledge of the examiner as to which patient subsequently developed a disciform lesion in that eye; (2) all findings were tape-recorded at first, so that no pattern could be observed from the record form before the investigation was completed; (3) repeatability tests were performed. After completion of the study, patients who developed a disciform lesion in the second eye were identified (group I) and compared with those patients who remained at the predisciform stage (group II). The results were analysed with the aid of a computer, using the x2 method. Results I. DRUSEN Drusen were found in all the patients studied. Number and distribution No significant difference in number of drusen was found between the two groups. This was so both in the macular and perimacular areas. Size Small drusen (less than 5 jum) were found more commonly and large drusen (5 to 8,Lm) less so in eyes which remained free of disciform lesions (group II) than those which developed a disciform lesion (group I), though at a low level of significance (P=-27 and -844 respectively). Z. Gregor, A. C. Bird, and I. H. Chisholm Patients who subsequently developed disciform degeneration (group I) had more areas of confluent drusen than patients in group II. The difference is highly significant (P<-1). All of the 13 patients with confluent drusen in the second eye followed up for more than 2 years developed a disciform lesion in this eye. The incidence of second eye involvement was 5 of 9 followed for 2 years and 3 of 16 followed for 1 year. Demarcation from surrounding retina No significant difference in prognosis was found between drusen with well-defined or blurred edges. II. FLUORESCEIN ANGIOGRAPHIC APPEARANCE Accumulation of dye in the late venous phase was observed more frequently in patients who subsequently developed disciform degeneration. The difference between the two groups is highly significant (P= 1). The incidence of second eye involvement in those patients with dye accumulation was 18 of 27 in those patients followed for over two years, 6 of 14 followed up for 2 years, and 3 of 18 followed for 1 year. Conversely, drusen which gave rise to no change in the background choroidal fluorescence were found more commonly in group II than in group I (P=-22). There was no significant difference between the two groups with regard to transmission defect. III. PIGMENT EPITHELIAL CHANGES No significant difference between the two groups was found for pigment clumping on the surface of drusen or unassociated with drusen. Subsequent development of disciform degeneration Of the 29 patients who subsequently developed a disciform lesion in the second eye the origin of the subretinal neovascular tissue could be related to preexisting lesions in. In 2 patients the neovascular tissue arose at the site of drusen with accumulation of dye (Figs. 5 and 6). In 5 patients neovascularisation occurred in areas which originally showed mainly transmission defects as well as some accumulation of dye (Fig. 7). One patient developed a disciform lesion in an area which appeared normal on the original angiogram. The origin of the neovascular tissue could not be identified in the remaining 3 patients; in 2 the neovascularisation involved the entire macular and paramacular areas, and in 1 the relevant fluorescein study was not available. Comments These results suggest that patients with unilateral disciform lesions are at high risk of developing a

5 Senile disciform macular degeneration in the second eye 145 (5a) (5b) Fig. 5 Development of disciform degeneration in the right eye of a 68-year-old woman. August 1974: vision with the right eye 6/12 and in the posterior pole there were multiple confluent drusen (Sa). Fluorescein angiogram showed intense hyperfluorescence corresponding to temporal drusen (Sb). February 1975: vision with the right eye 6/36 with serous detachment of the posterior pole, subretinal haemorrhage and dye leakage from subretinal neovascular tissue in an area corresponding with the dye accumulation (5c) (5c) lesion in the second eye if there are large confluent drusen in which there is progressive leakage of dye on fluorescein fundus angiography. Conversely, if drusen are small and do not alter the pattern of the background choroidal fluorescence, the risk of visual loss in the second eye is relatively less. It is likely that the large areas of subpigment epithelial white deposits which we have termed confluent drusen are similar to the basal linear deposits described by Sarks (1976). The significance of accumulating fluorescence within drusen is uncertain. It is acknowledged that penetration of Bruch's membrane by choroidal blood vessels occurs more commonly than is clinically evident, particularly in areas of accumulation of abnormal material on the inner surface of Bruch's membrane (Sarks, 1976). Blood vessels within drusen would certainly account for dye accumulation during angiography, and it is thus not surprising that this clinical finding should indicate a poorer visual prognosis. These findings are important in defining the risk of disciform degeneration in a second eye, and also in the design of clinical trials to determine whether photocoagulation alters the incidence of disciform

6 146 Z. Gregor, A. C. Bird, and L H. Chisholm (6a) (6b) Fig. 6 Development of disciform degeneration in the left eye of a 67-year-old woman. February 1974: vision with the left eye was 6/9. In the posterior pole there were large drusen, confluent in places (6a). Fluorescein angiogram showed transmission of choroidal fluorescence and accumulation of dye inferiorly (6b). November 1974: vision with the left eye 6/24. There was a serious detachment of the posterior pole and dye leakage from subretinal neovascular tissue and subretinal haemorrhage (5c) (6c) degeneration developing in an eye with drusen. Having identified high- and low-risk factors, these characteristics should be recorded, and ideally the patients stratified in respect of these factors before they are randomised. We should like to thank Mr K. S. Sehmi for his photographic expertise and Miss J. Fisher for her secretarial assistance. We are particularly grateful to Mr H. Donovan, who undertook the statistical analysis. References Brown, E. V. L. (194). Retroretinal tissue from the choroid in Kuhnt-Junius degeneration of the macula. Anatomic study. Archives of Ophthalmology, 23, Chandra, S. R., et al. (1974). Natural history of disciform degeneration of the macula. American Journal of Ophthalmology, 78, Donders, F. C. (1855). Beitrage zur pathologischen Anatomie des Auges. Albrecht von Graefes Archivfur Ophthalmologie, 1, abt. 2, Friedman, E., Smith, T. R., and Kuwabara, T. (1963). Senile choroidal vascular patterns and drusen. Archives of Ophthalmology, 69,

7 Senile disciform maciular degeneration in the second eye 147 (7a) (1b) Fig. 7 Development of disciform degeneration in the left eye of a 62-year-old woman. May 1971: vision in the left eye was 6/6 and in the posterior pole there were confluent drusen (7a). Fluorescein angiogram showed transmission of choroidal fluorescence as well as accumulation ofdye (7b). July 1972: vision with the left eye 6/36 with serous detachment of the posterior pole and dye leakage from subretinal neovascular tissue (7c) (7c) Gass, J. D. M. (1973). Drusen and disciform macular detachment and degeneration. Archives of Ophthalmology, 9, Gifford, S. R., and Cushman, B. (194). Certain retinopathies due to changes in the lamina vitrea. Archives of Ophthalmology, 23, Hogan, M. J. (1967). Bruch's membrane and disease of the macula. T-ansactions of the Ophthalmological Societies of the United Kingdom, 87, Hogan, M. J., Alvarado, J., and Weddell, J. E. (1971). Histology of the Human Eye; an Atlas and Textbook, pp Philadelphia, Saunders. Riechling, W., and Klemens, F. (194). Ober eine gefass- fuhrend Bindegewebsschicht zwischen dem Pigmentepithel der Retina und der Lamina Vitrea. Albrecht von Graefes Archives fur Ophthalmologie, 141, Sarks, S. A. (1973). New vessel formation beneath the retinal pigment epithelium in senile eyes, British Journal of Ophthalmology, 57, Sarks, S. A. (1976). Ageing and degeneration in the macular region: a clinico-pathological study. British Journal of Ophthalmology, 6, Teeters, V. W., and Bird, A. C. (1973). The development of neovascularisation of senile disciform macular degeneration. American Journal of Ophthalmology, 76, 1-18.

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