Brit. 7. Ophthal. (I975) 59, 710

Evolution of the retinal black sunburst insickling haemoglobinopathies

GEORGE ASDOURIAN, KRISHAN C. NAGPAL, MICHAEL GOLDBAUM,DIMITRIOS PATRIANAKOS, MORTON F. GOLDBERG, AND MAURICE RABBFrom the Sickle Cell Eye Clinic of the University of Illinois Eye and Ear Infirmary, Chicago, Illinois

Black sunbursts are circular black chorio-retinalscars with stellate or spiculate borders, commonlyfound in the peripheral fundi of patients withsickle haemoglobinopathies. They are possibly foundless frequently in patients with SC and sicklethalassaemia (Sthal) haemoglobinopathies (Welchand Goldberg, I966), although in an unselectedseries the reported incidence of black sunbursts andsimilar pigmented lesions was 32 per cent of SSpatients (Condon and Serjeant, 1972a), 20 per centof Sthal patients (Condon and Serjeant, I972b),and 4I per cent of SC patients (Condon and Ser-jeant, I972C). Although haemorrhages and choroidalvascular occlusions have been considered as causesof these lesions (Okun, I969; Wise, Dollery, andHenkind, 1971; Condon and Serjeant, 1972 a, b, c;Romayananda, Goldberg, and Green, 1973; Cogan,1974) their pathogenesis has not been well docu-mented.

This report documents the evolution of theselesions in three patients who were studied pro-spectively during a period of 3 years.

MethodsDuring the last 3 years the Sickle Cell Eye Clinic of theUniversity of Illinois Eye and Ear Infirmary screenedsome 400 patients with different sickling haemoglo-binopathies. Of these patients, 38 who revealed theearliest stages of sickling retinopathy (stage I, peripheralarteriolar occlusions; and stage II, peripheral arterio-venous anastomoses) (Goldberg, 1971) were included ina longitudinal study to evaluate the natural course andevolution of lesions characteristic of sickling retino-pathies. Studies of these patients included a generalocular examination, indirect ophthalmoscopy, detailedfundus drawings, colour fundus photography, andfluorescein angiography of 3600 of the equatorial andperipheral fundus. Ophthalmoscopy, photography,and fluorescein angiography were repeated every 3 to 4mth.

Address for reprints: Morton F. Goldberg, MD, University ofIllinois, Eye and Ear Infirmary, I855 W. Taylor Street, Chicago,Illinois, 6o6I2, USA

ResultsDuring the period of observation three patients de-veloped black sunburst lesions in retinal areas that hadbeen documented by photography as normal at thestart of the observation period.

CASE REPORTS

Case i

A 1g-year-old black man with sickle cell haemoglobinC disease, was initially screened at the Sickle CellEye Clinic on 3 October I972. Haemoglobin electro-phoresis revealed haemoglobin S of 54-2 per cent andhaemoglobin C of 45-8 per cent. The haemoglobin levelwas I3-9 g/ioo ml, and the haematocrit reading 40-4per cent.The ocular history was unremarkable and corrected

visual acuity was 20/25 in each eye. The conjunctivadid not reveal the sickling conjunctival sign (Paton,I962). Ophthalmoscopy revealed a variety of nonproli-ferative retinal lesions including retinal haemorrhages(salmon patches), chorio-retinal scars (black sunbursts),and schisis-like cavities containing iridescent spots.Both ophthalmoscopy and fluorescein angiographydemonstrated extensive areas of stage I (arteriolarocclusions) and II (arterio-venous anastomoses) lesions(Goldberg, I971) involving the majority of the equatorialretina in each eye. The patient was recruited into thelongitudinal study and he has been examined every 3mth with indirect ophthalmoscopy, colour fundusphotography, and fluorescein angiography. On hisinitial examination in October 1972, the 12 o'clockmeridian of the right eye did not reveal any abnornali-ties (Fig. I a). In November 1973, he had multiplepreretinal and intraretinal haemorrhages at differentstages of resorption. One of these lesions at the 12o'clock meridian revealed gradual resorption of thehaemorrhage (Fig. ib). When he was seen in July I974,early pigmentary changes were evident (Fig. ic). Twoareas in the left retina at the I and 4 o'clock meridianshad initially revealed no abnormalities. In JanuaryI973 intraretinal haemorrhages were observed in theseareas (Figs 2a, 3a). The haemorrhages were largeenough to dissect into the overlying vitreous. After 6mth these areas showed absorption of the haemorr-hages with the progressive development of pigmentarychanges (Figs 2b, 3b).

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Evolution of the retinal black sunburst 711

Case 2

A 27-year-old black man with sickle cell thalassaemia,was screened at the Sickle Cell Eye Clinic. He had noocular symptoms; haemoglobin electrophoresis revealedhaemoglobin S of 72-8 per cent, A2 of 5-2 per cent, andF of 22 per cent. The haemoglobin level was I5 g/I00 mland the haematocrit reading was 43 per cent. The visualacuity was 20/15 in both eyes. The conjunctiva did notreveal the conjunctival sickling sign (Paton, I962).Ophthalmoscopy revealed stage I and stage II retino-pathy (Goldberg, 1971) in the right eye. Ophthalmoscopyof the left eye revealed stage I, II, and III (sea-fanneovascularization) retinopathy (Goldberg, 197I). Fluo-rescein angiography of the right eye confirmed the

FIG. I Case i, right eye. (a) Normal-appearing12 o'clock meridian in October 1972. Arrowindicates site offuture intraretinal haematoma.(b) Same area after i yr with evidence of resorbingintraretinal haemorrhage. Haemorrhage has alsobroken into vitreous, causing slight haze. (c) Samearea in July 1974. Pigmentary changes haveappeared in centre of lesion with evidence ofschisis cavity around it

presence of arteriolar occlusions and arterio-venousanastomoses. Fluorescein angiography of the left eyerevealed occluded arterioles and arterio-venous anas-tomoses as well as perfusion and leakage of dye from thesea fan. On follow-up examination, the i i o'clock areaof the left eye, which had been initially normal, showedan intraretinal haemorrhage, which io mth later starteddeveloping pigmentation characteristic of black sun-bursts.

Case 3A 23-year-old black man with sickle cell haemoglobinC disease, was seen at the Sickle Cell Eye Clinic on5 December 1972, with a history of blurred vision in

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(2b)

FIG. 2 Case I, left eye. (a) i o'clock meridian in January

1973 revealing intraretinal haemorrhage with overlyingvitreous haze. Arrow indicates reference vessel (see Fig.2b). (b) Same area after 6 mth. Chorio-retinal scar withiridescent spots has resulted. Smaller arrows indicateboundaries of schisis cavity caused by resorption ofhaematoma. Larger arrow indicates reference vessel (seeFig. 2a)

the right eye. Haemoglobin electrophoresis revealedhaemoglobin S of 53-I per cent and haemoglobin C of46-9 per cent.

Corrected visual acuity was 20/30 in the right eye

and 202/5 in the left eye. There was no conjunctivalsickling sign. Ophthalrnoscopy revealed stage I, II, andIII retinopathy in both eyes and evidence of an old

vitreous haemorrhage in the right eye. The patient wassubsequently admitted to hospital several times and theneovascularization was treated with cryotherapy.Of interest was an area at the 2 o'clock meridian in

the right eye. At the initial examination this area ap-peared to be normal (Fig. 4a). One year later there wasevidence of a previous intraretinal haemorrhage (Fig.4b). Two years after the initial examination this arearevealed the start of pigmentation characteristic of ablack sunburst (Fig. 4c).Another area of interest in this patient was the 9

o'clock meridian of the same eye. In February 1973,an intraretinal haemorrhage (salmon patch) was evidentadjacent to a well-developed, small black sunburst. Onemth later there was gradual absorption of the hae-morrhage and 7 mth later minimal pigmentary changeswere evident.

DiscussionBlack sunbursts are circular black chorio-retinalscars that characteristically occur in the fundi ofpatients who have various types of sickle cellanaemia. These well-developed lesions have typicalfeatures distinguishing them from somewhatsimilar-appearing inflammatory lesions; the sun-bursts are usually round or ovoid, ranging in sizebetween o 5 and 2 disc diameters, and are charac-teristically located in the equatorial fundus. Theyusually have stellate or spiculate borders and arefrequently associated with refractile yellowishgranules. Their configurations range from tinypigmented spots to large multi-spiculated scars(Fig. 5 a-c). Because of their characteristic peri-pheral location these lesions usually do not interferewith vision.

Histologically, these lesions represent areas offocal retinal pigment epithelial hypertrophy, hyper-plasia, and migration. Occasionally there is a dis-tinct perivascular localization of the pigment inthe sensory retina. The sensory retina is thinnedand degenerated with loss of its lamellar architec-ture. Pigmented, haemosiderin-laden macrophagesand diffuse deposition of iron are also found inthese lesions (Romayananda and others, 1973).The pathogenesis of these lesions has remained

speculative. Retinal arteriolar occlusions hadpreviously been incriminated because of thepresence of arterioles which apparently suppliedthe area of the retina involved by the sunbursts(Welch and Goldberg, I966); however, arteriolarfeeders could not be found in all cases. A blow-outof preretinal, intraretinal, or subretinal haemorr-hage, with subsequent reparative processes in theretina, had also been proposed as the cause of theblack sunburst lesions (Okun, I969; Condon andSerjeant, 1972b; Romayananda and others, I973).Okun (I969) reported a case where an initial

salmon-coloured preretinal haemorrhage, whichwas accompanied by adjacent subretinal bleeding,

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Evolution of the retinal black sunburst 713

FIG. 3 Case i, left eye. (a) 4 o'clock meridian in January I973 revealing large intraretinalhaemorrhage which has dissected into vitreous. (b) Same area after 6 mth. Characteristicsunburst has resulted

FIG. 4 Case 3, right eye. (a) 2 o'clockmeridian. Retina is normal. (b) One yr latersame area reveals schisis cavity withiridescent spots (evidence of previousintraretinal haemorrhage). (c) Same areaafter 2 yr. Pigmentary changes are evident

subsequently disappeared to leave a brownish areawith iridescent spots. This was called a chorio-retinal scar, but there was no evidence of excessivepigment and no further follow-up examinationsof the area were made.

In each case, the black sunburst began as anintraretinal haemorrhage, probably because of asudden arteriolar occlusion with subsequent necro-sis of the distal arteriolar wall and marked leak-age of erythrocytes through the damaged wall.

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(5a)(5c)

(5b)

The intraretinal haemorrhage was large enoughto dissect into the vitreous in some cases, and italso apparently dissected through the photorecep-tors into the potential space between the sensoryretina and the pigment epithelium (the subretinalspace). Evidence of retinal haemorrhage dissectinginto the subretinal space has also been docunmentedin angiomatosis retinae (Goldberg and Duke,I968). The presence of blood adjacent to the retinalpigment epithelium presumably stimulates it toproliferate and migrate. With the absorption ofthe small haematoma within the sensory retina,schisis cavities develop. Iridescent spots, which

FIG. 5 (aC) Different configurations of well-developedblack sunbursts

represent iron-laden macrophages, are often foundwithin these cavities. The cavities surroundingthe sunburst remain as evidence of the initiatingintraretinal haematoma.The absence of the retinal vasculature surround-

ing certain black sunbursts is readily explained bythe known repetition in sickling patients of arterio-lar occlusions and proximal propagation of intra-vascular clots with drop-out of surrounding capil-laries. Some sunbursts are therefore left in areasof avascular retina with no apparent connexionsto the adjacent retinal vasculature.

Certain intraretinal haemorrhages, on the other

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Evolution of the retinal black sunburst 715

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Block sunburstFIG. 6 Schematic interpretation showing a salmon patch haemorrhage becoming schisis cavity and (b) large intraretinalhaemorrhage dissecting into subretinal space and turning into black sunburst. ILM, internal limiting membrane; SR,sensory retina; RPE, retinal pigment epithelium; CC, choriocapillaris; C, choroid

hand, do not dissect into the subretinal space.Their resorption leaves behind schisis cavitieswith iridescent spots, but without evidence ofpigmentary disturbance (Fig. 6).The causative role of retinal arteriolar occlusions

has been disputed by some authors with the argu-

ment that branch and central retinal artery occlu-sions are never associated with pigment alterations(Wise and others, 197I; Cogan, I974). However,in these circumstances, the retinal pigment epi-thelium is not traumatized and therefore does notrespond by proliferation or migration. Interferencewith the choriocapillaris circulation has beensuggested as the cause of black sunbursts (Wiseand others, 197I; Cogan, 1974), but evidence forthis hypothesis is lacking. Fluorescein angiographvis usually of no great diagnostic help during theacute stage, when the haemorrhage obscures theinvolved vessels. In healed lesions fluoresceinangiography reveals areas of hyper- and hypo-Fluorescence depending on the amount of pigmentclumping and pigment dispersion (Fig. 7). Adjacentcapillary bed drop-out is usually present, and isevidence of previous retinal vasculature occlusion.In many cases the major arteriole responsible forthe initial blow-out haemorrhage can also be seen.

Acute occlusions of choroidal capillaries dooccur in other cases and have been noteworthy inpatients with severe systemic hypertension. Theseocclusive phenomena result in pigmented areas

in the fundus known as Elschnig's spots (Klien,i968; Morse, 1968; Burian, I969), which differ

from the black sunburst lesions, clinically as wellas pathologically. Clinically, the typical, healedElschnig spot is an isolated, round, yellowisharea, one-sixth to one-third the papillary diameterwith a pigmented centre. It is most commonlyseen in the vicinity of the optic disc or the retinialmidperiphery. Black sunbursts are usually largerand are generally located at the retinal equator.A characteristic sunburst in the posterior pole has

FIG. 7 Case i, Fluorescein angiogram of black sunburst(cf. Fig. I c). Pigmentary changes evident as hypo- or

hyperfluorescent areas. Capillary abnormalities evident.No neovascular tissue or leakage of dye

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7I6 British Journal of Ophthalmology

yet to be seen. Pathologically, the differencesbetween these lesions are even more marked. AnElschnig spot represents a clump of pigment;the surrounding depigmented epithelial cellsconstitute the yellow-orange halo. The chorio-capillaris shows foci of fibrosis, obliteration, andresidual ghost capillary outlines. The overlyingsensory retina is usually normal. In contrast, theyellowish halo around the black sunburst repre-sents the boundaries of a schisis cavity that oftencontains iron-laden macrophages; the chorio-capillaris does not show any occlusive phenomenaand the retinal architecture is distorted becauseof the previous intraretinal haemorrhage. Theblack sunburst also differs in several respects fromthe extensive chorio-retinal degenerations thathave been reported to be the sequelae of ciliaryand choroidal artery occlusions (Condon, Serjeant,and Ikeda, I973), in that the latter lesions occupylarge sectoral areas of the fundus. They are alsocharacterized by advanced choroidal and retinalpigment epithelial atrophy with a grey-greenbackground, through which choroidal vessels areusually visible.

In the differential diagnosis of the black sunburstone should also consider inflammatory diseasethat can cause chorio-retinal scars, such as toxo-plasmosis, syphilis, and presumed histoplasmosis.

'oxoplasmic chorio-retinal scars are often foundin the posterior pole as well as the retinal periphery.Apart from differences of localitv, these lesionsare often characterized by extensive fibrosis or byintense pigment proliferation and clumping aroundtheir periphery, leaving a central atrophic regionthrough which the choroid and sclera are exposed.Satellite scars are sometimes present. The retinallesions in presumed histoplasmosis are very small,punched-out, pale, slightly pigmented, discretefoci, and are usually located in the retinal peri-phery. Disseminated chorio-retinitis as a result ofsyphilis may be manifested as varying types ofchorio-retinal pigmentation, irregular masses, anddispersed or confluent areas of scarring. Pigmentsheathing of veins and narrowing of retinal arteriesare often present (Ballantyne and 'Michaelson,1973).

SummaryIn a prospective study of 38 patients, who wereinitially selected as being at an early stage ofsickling retinopathy, three developed circular blackchorio-retinal scars (black sunbursts) during aperiod of 6 to 24 months. These lesions appear tobe the sequelae of intraretinal and subretinalhaemorrhage. They occur in the fundus peripheryand do not interfere with vision.

References

BALLANTYNE, A. J., and MICHAELSON, I. C. (1973) 'Textbook of the Fundus of the Eye'. Williams & Wilkins,Baltimore

BURIAN, H. M. (I969) Amer. J. Ophthal., 68, 4I2COGAN, D. G. (I974) 'Ophthalmic Manifestations of Systemic Vascular Disease'. Saunders, PhiladelphiaCONDON, P. I., and SERJEANT, G. R. (1972a) Amer. Y. Ophthal., 73, 533

(1972b) Ibid., 74, 1105(1972C) Ibid., 74, 921,and IKEDA, H. (I973) Brit. J. Ophthal., 57, 8i

GOLDBERG, M. F. (1971) Invest. Ophthal., 12, 633, and DUKE, J. R. (I968) Amer. J. Ophthal., 66, 693

KLIEN, B. A. (I968) Ibid., 66, I069MORSE, P. H. (I968) Ibid., 66, 844OKUN, E. (I969) Docum. ophthal. (Den Haag), 26, 574PATON, D. (1962) Arch. Ophthal., 68, 627ROMAYANANDA, N., GOLDBERG, M. F., and GREEN, W. R. (1973) Trans. Amer. Acad. Ophthal. Otolaryng., 77, 652WELCH, R. B., and GOLDBERG, M. F. (I966) Arch. Ophthal., 75, 353WISE, G. N., DOLLERY, C. T., and HENKIND, P. (197) 'The Retinal Circulation'. Harper & Row, New York

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