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Show ORIGINAL CONTRIBUTION Asymptomatic Peripapillary Subretinal Hemorrhage: A Study of 10 Cases Patrick Sibony, MD, Stuart Fourman, MD, Robert Honkanen, MD, and Fadi El Baba, MD Background: Peripapillary subretinal hemorrhage (PSH) is often found together with optic disc drusen, optic disc edema, peripapillary subretinal neovascu-lar membranes, vitreous traction, and bleeding diatheses. Previous reports have stated that such optic disc hemorrhages are associated with intra-papillary bleeding largely in patients of Asian origin who are visually symptomatic from this process. We have encountered patients with PSH who have clinical features that differ from those described in these reports. Methods: This is a retrospective observational case series. Medical records of 10 patients with isolated peripapillary subretinal hemorrhages were reviewed for clinical characteristics and ancillary testing, including demographics, history, complete eye examination, visual fields, fundus photos, ultrasound, and fluorescein angiography (four patients) at pre-sentation and follow-up. We excluded patients with drusen, neovascular membranes, disc edema, and intrapapillary hemorrhages. Results: There were 10 patients, all white women without visual symptoms, who had isolated, monoc-ular, nasal, or superonasal peripapillary subretinal hemorrhage, a dysplastic crowded-tilted optic disc, myopia, and normal visual function. The hemorrhages resolved without sequelae over 3-6 months. The findings were frequently discovered on routine examination and suspected of representing papilledema. Conclusions: We have described a benign syndrome of isolated PSH in crowded and tilted optic discs in myopic eyes of white women. The PSHs do not cause visual symptoms and resolve spontaneously. We propose that an interplay of ocular motor forces, scleral thinning, and vitreopapillary traction acting Department of Ophthalmology State University of New York at Stony Brook University Hospital and Medical Center Stony Brook, Stony Brook, New York. Address correspondence to Patrick Sibony, MD, SUNY Stony Brook, Health Sciences Center, Stony Brook, NY 11794-8223; E-mail: patrick. sibony@stonybrook.edu on a morphologically vulnerable optic disc explains these hemorrhages. (J Neuro-Ophthalmol 2008;28:114-119) Peripapillary subretinal hemorrhages (PSHs) have been described in patients with optic disc drusen(l-4), optic disc edema (5-7), peripapillary subretinal neovascular membranes(8,9), and bleeding diatheses (10). A clinical syndrome also has been reported that is characterized by the spontaneous onset of an intrapapillary hemorrhage that extends into the adjacent subretinal peripapillary region and occurs in patients who are Asian and myopic and have mildly dysplastic optic discs (11-13). These hemorrhages resolve after several months; the visual prognosis is favorable. In a review of our patients with peripapillary subretinal hemorrhages, we have identified a variant of this syndrome in white women who have uniocular asymp-tomatic peripapillary (but not intrapapillary) subretinal hemorrhages, crowded tilted optic discs, and myopia. The purpose of this report is to describe the clinical character-istics of this group of patients, to review pathogenic mechanisms, to propose additional contributory factors in the genesis of these hemorrhages, and to emphasize the asymptomatic benign course of a syndrome that may mimic papilledema. METHODS Ten patients with isolated peripapillary subretinal disc hemorrhages referred for neuro-ophthalmic examina-tion between February 1995 and November 2005 were identified from a departmental database. We excluded patients with associated intrapapillary, vitreous, or nerve fiber papillary hemorrhages. Patients with optic disc edema, papillitis, ischemic optic neuropathy, drusen, and juxtapapillary subretinal neovascular membranes were also excluded. Medical and ocular history, past history, ocular examination, and ancillary testing were retrospectively reviewed for each patient. From the patients' medical charts, we extracted information about age, gender, ethnicity, presenting symptoms, systemic disease, medications, 114 J Neuro-Ophthalmol, Vol. 28, No. 2, 2008 Peripapillary Subretinal Hemorrhage J Neuro-Ophthalmol, Vol. 28, No. 2, 2008 refractive error, acuity, color vision, pupillary examination, visual fields, evidence of vitreous traction or detachment, and ancillary testing including B-scan to exclude drusen and assess vitreous attachment to the disc (10 patients), fundus photos (10 patients), and fluorescein angiography (4 patients). Follow-up documentation of complete resolution of the hemorrhage was available in 9 of the 10 patients. The study was reviewed and approved by the Stony Brook Institutional Review Board for Human Studies. RESULTS Ten patients with isolated PSHs who met the inclusion criteria were identified. Their clinical features are summarized in Table 1. Ages ranged from 8 to 64 years (mean, 39 years). All were white women. One patient (Case 5) complained of a subjective blur in both eyes, one patient (Case 9) complained of unrelated headaches; all others were asymptomatic. Six of the patients had no significant prior medical problems. One patient was examined 5 months postpartum, one had a history of an intracranial aneurysm treated 7 years earlier, one had ulcerative colitis with a small asymptomatic parasagittal meningioma, and one had hypertension. Three of the patients had previously undergone a lumbar puncture for suspected idiopathic intracranial hypertension, and all had normal opening pressures. None of the patients was taking antiplatelet medications or had a history of bleeding problems. All patients had been referred for neuro-ophthalmic consulta-tion to evaluate the optic discs for papilledema or buried drusen. Nine of the affected eyes were myopic with a mean spherical equivalent of 4.80 diopters; five eyes had high myopia (spherical equivalents between 6.50 and 8.63 diopters) and mild ophthalmoscopic signs of myopia. One patient (Case 10) was mildly hyperopic. Visual acuity, color vision (tested by Ishihara plates), pupils, slit lamp examination, and eye movements were always normal. On Humphrey visual field testing 4 of the 10 patients showed mild enlargement of the blind spot, but otherwise there were no abnormalities. None of our patients had visible signs of optic disc drusen by ophthalmoscopy or by ultrasonography. Two patients had complete posterior vitreous detachments with Weiss rings observable by ophthalmoscopy. One patient had a partial posterior vitreous detachment as determined by B-scan ultrasonography. All affected optic discs were crowded with small or absent cups (Figs. 1 and 2). All optic discs exhibited variable degrees of tilting (oblique insertion) with elevation and blurring of the nasal or superonasal regions of the nerve TABLE 1. Features often cases with asymptomatic peripapillary subretinal hemorrhage Case number Age Refractive error Acuity Months to resolve 1 2 3 4 5 6 7 8 9 10 58 8 64 56 10 35 20 50 28 63 -6.50 + 1.00 X 90 -7.00 + 1.00 X 90* -3.75 + .75 X 5 -3.75 + 1.00 X 175* -7.00 + 1.75 X 110 -7.00 + 1.75 X 75* -3.00* -3.00 -1.50 + .25 X 135 -1.50 + .50 X 180* -9.25 + 1.25 X 125* -10.25 + 1.50 X 145 -8.00 + .50 X 90* -6.50 + .50 X 90 -7.50 + .50 X 3* -8.50 + 1.25 X 10 -1.75* -1.50 + .25 X 170 + 1.00 + .75 X 140 + 0.25 + 1.00 X 65* 20/25 20/25 20/25 20/20 20/20 20/20 20/20 20/20 20/20 20/20 20/25 20/25 20/30 20/20 20/20 20/25 20/25 20/20 20/20 20/30 5 5 6 [5 yrs later] No follow-up 3 4 6 5 4 All patients were white females. *Affected eye. 115 J Neuro-Ophthalmol, Vol. 28, No. 2, 2008 Sibony et al FIG. 1. Fundus photographs of optic discs of Cases 1-9. Peripapillary subretinal hemorrhages are indicated by a small black arrowhead. Note that all hemorrhages are located nasally or superonasally. Focal nasal whitening is best demonstrated in Cases 8 and 9 {white arrowhead). The optic discs are crowded with small or absent cups and tilting with blurred elevation of the nasal or superonasal half of the optic disc. Myopic crescents are evident in Cases 1, 2, and 6-9. The superior pole of the optic disc is rotated temporally in Cases 1 and 6. head. Temporal or inferotemporal crescents were visible in discs in the fellow eyes, except in Case 10, were similarly 7 patients (Cases 1, 3, and 6-10). Peripapillary atrophy on crowded and tilted. the nasal side of the optic disc was visible in two patients In all cases, the PSH was uniocular (five in the right (Cases 6 and 7). Variable degrees of focal whitening {white eye and five in the left eye). The PSH was located along the arrowheads in Cases 8, 9, and 10 in Figs. 1 and 2) along the nasal or superonasal margin, spanning 1/4 to 3 clock hours of superior and nasal margins of the optic disc were observed the optic disc circumference and varying from a thin line to in seven patients (Cases 2, 3, 5, 6, and 8-10). The optic a third of the disc diameter in width. The hemorrhages in 116 © 2008 Lippincott Williams & Wilkins Peripapillary Subretinal Hemorrhage J Neuro-Ophthalmol, Vol. 28, No. 2, 2008 FIG. 2. Case 10. Fundus photograph (A) shows crowded tilted disc with nasal peripapillary subretinal hemorrhage. The optic disc is obliquely inserted, elevated nasally, and slightly rotated with a small inferotemporal crescent. The nasal disc margin is blurred and focally whitened (white arrowhead). Fluorescein angiography in the early phase (B) shows blocked fluorescence and in the late phase (C) shows staining of the nasal part of the optic disc. two patients with atrophic nasal crescents were located at the boundary between the edge of normal retina and the edge of the crescent (Cases 1 and 7). No patient had intrapapillary, nerve fiber layer, or vitreous hemorrhages, and no patient had a vitreopapillary remnant. Four patients underwent fluorescein angiography. A representative fluorescein study is shown in Figure 2 (Case 10, middle, right). The choroidal flush was initially blocked by the hemorrhage. An area of peripapillary hyperfluorescence became visible during the late stages of laminar venous filling between 30 and 60 seconds and fully developed by 3 minutes. In all patients, late staining of the nasal and superior peripapillary region adjacent to the hemorrhage was noted to extend variably into the periph-eral disc margin. No patient showed diffuse leakage of the optic disc, telangiectasia of the disc vessels, micro-aneurysms, or intrapapillary hemorrhages. No patient who underwent fluorescein angiography displayed signs of vascular disc anomalies or subretinal neovascular membranes. The PSH resolved over a period of 3-6 months in eight patients. One patient, who failed to follow up, was examined 5 years later (Case 4), by which time the hemorrhage had resolved. One patient was lost to follow-up (Case 5). DISCUSSION We have described 10 white women with asymp-tomatic, spontaneously acquired, uniocular, nasal or superonasal PSH. All had crowded tilted optic discs with normal corrected visual acuity. Nine of 10 patients were myopic. The hemorrhages resolved without sequelae over 3-6 months where follow-up was available. Our patients had findings similar in some respects to those with the syndrome of intrapapillary hemorrhage with adjacent peripapillary subretinal hemorrhage (IHAPSH) described by Cibis (11), Kokame et al (12), and Katz and Hoyt (13) and in Japanese medical journals (14-18). The common findings have included the nasal location of the hemorrhage, myopia, mildly dysplastic optic discs, normal visual function, and complete disappearance of the hemorrhage without sequelae. However, there are several characteristics that distinguish our series from the previous reports. Nearly all of previously described patients were visually symptomatic from floaters or blurred or hazy vision, whereas our patients were visually asymptomatic. None of our patients had intrapapillary hemorrhages, a prominent feature observed in all previous reports (11- 13). Kokame et al (12) suggested that the PSH was an extension of a primary intrapapillary hemorrhage. How-ever, our patients demonstrate that PSH can occur without an intrapapillary hemorrhage. The observation of partial posterior vitreous detachments among seven of the eight patients reported by Katz and Hoyt (13) led them to conclude that the papillary and peripapillary subretinal hemorrhages were caused by vitreopapillary traction. However, Kokame et al (12) were unable to confirm this finding by biomicroscopy (10 eyes), by B-scan ultraso-nography (4 eyes), or by optical coherence tomography (2 eyes). Seven of our patients had no signs of vitreous traction or detachment by ultrasound when the hemorrhage was visualized. Lastly, patients with IHAPSH have been Asian, whereas our patients were white women. We suspect that there is a continuum linking both groups of patients and that the syndrome of IHAPSH should be broadened. As pathogenetic mechanisms of IHAPSH, Kokame et al (12) and Katz and Hoyt (13) proposed vitreopapillary traction, hemorrhage from anatomically vulnerable prel-aminar blood vessels in crowded optic discs, hemodynamic 117 J Neuro-Ophthalmol, Vol. 28, No. 2, 2008 Sibony et al effects of the Valsalva maneuver, and complications of optic disc edema. No single mechanism explained all reported cases. Based on the following information, we hypothesize that the cause of PSH is multifactorial. A dysplastic crowded disc with a small or absent cup and elevation of the nasal or superonasal portion of the disc (tilting) has been a common finding among reported patients with IHAPSH (12,13,19-21) and was evident in all of our patients. The optic nerves are obliquely inserted. The nerve fibers enter through a small scleral ring along an acutely angled pathway into the nasal retina. Temporal fibers gently bend over the scleral rim (21,22). Fluorescein angiography of the optic disc of our patients displayed late focal staining of the nasal and superior peripheral region of the disc but no evidence of optic disc edema. Others have also observed this pattern (12,13). Small crowded discs are vulnerable to vascular complications frequently observed in nonarteritic anterior ischemic optic neuropathy, even among patients without vascular risk factors (23-29). Patients with crowding due to optic disc drusen can develop PSH, neovascular mem-branes, ischemic optic neuropathy, and retinal vein occlu-sions (1,3,4,30). Although the precise mechanism of bleeding in patients with isolated PSH or IHAPSH is unknown, it has been suggested that the blood vessels of the nasal and superonasal regions of the disc are structurally vulnerable (12,15,17). Vessels from the peripapillary choriocapillaris, choroidal branches that supply the pre-laminar nerve head or branches of the posterior ciliary artery that traverse the Border tissue of Elschnig (31-33) in the nasal region of the disc, may be prone to stretching, kinking, or compression in these crowded tilted optic discs. Vitreopapillary traction also appears to play an important role in the genesis of PSH in at least some patients, especially when associated with an intrapapillary or vitreous hemorrhage (11,13). However, the absence of a partial posterior vitreous detachment among some of the patients reported by Kokame et al (12) and in seven of our patients indicates that there may be additional contributory biomechanical factors. The sclera in myopia is thinner and more distensible and therefore subject to stretching ("scleral creep") in response to extraocular muscle contractions and intraocular pressure, among other factors (19,34-36). Temporal cres-cents in myopia may also represent an early sign of globe expansion. Pruett et al (36) suggested that myopic lacquer cracks in Bruch's membrane are a mechanical consequence of scleral creep. Expanding lacquer cracks are sometimes preceded by subretinal hemorrhages in the posterior pole even in the absence of angiographically detectable subretinal neovascular membranes (42). Greene (37) compared the scleral canal to a hole in a plate under tension. Stress forces applied to such a plate are significantly amplified at the margins of the hole. Stress forces applied to the sclera by the extraocular muscles are magnified in the peripapillary region. In developing a mathematical model of the shear stress forces on the eye wall generated by saccadic movements, David et al (38) demonstrated that vibrational stress waves are amplified at the optic nerve head and increase significantly with thinning of the scleral wall. Adduction saccades are known to elicit transient, unilateral phosphenes temporal to fixation during the dark-adapted state (39). It has been suggested that these "flick phosphenes" are consequent to the inertial traction of the vitreous on the optic disc and surrounding retina (39,40). However, flick phosphenes are also observed by subjects with complete posterior vitreous detachments (41). These facts suggest that saccadic eye movements may mechanically strain the peripapillary retina even in the absence of vitreopapillary attachment. We propose that the similarities in optic disc mor-phology, myopia, and location of the subretinal hemor-rhages suggest that the isolated PSH we observed and the IHAPSH observed by others (11,13) are variants of the same underlying process. In both conditions, the optic disc hemorrhages are the result of an interplay of external forces generated by eye movements (37,38), thinning of the sclera (scleral creep)(36), and fractional forces of the vitreous (13) acting on a crowded tilted optic disc that may be mor-phologically predisposed to hemorrhage. Elevated venous pressure from a Valsalva maneuver or bleeding diathesis could increase the tendency to bleed. The relative con-tribution of each of these forces may influence the location of the optic disc hemorrhage. For example, vitreopapillary traction is more likely to result in intrapapillary, vitreous, or nerve fiber hemorrhages as described by Katz and Hoyt (13). Biomechanical stress due to eye movements and peripapillary thinning at the level of the choroid or sclera may predominate in patients with isolated PSH. Such biomechanical forces may also play a role in the genesis of glaucomatous optic atrophy (43), peripapillary neovascular membranes, and PSH in patients with optic disc drusen or papilledema. Clinicians should recognize that isolated uniocular PSH in crowded and tilted discs are often benign but also distinguish this condition from PSH associated with optic disc edema, drusen, and neovascular membranes. The pres-ence of myopia, nasal location of the hemorrhage, pre-servation of visual function, characteristic disc morphology, and late staining of the nasal disc margin on fluorescein angiography should establish the diagnosis. Atypical location of the hemorrhage, dilated telangiectatic vessels, micro-aneurysms, and diffuse late leakage into the optic disc are more typical of optic disc edema. Ophthalmoscopy, ultraso-nography, or CT can be used to confirm the presence of buried drusen. 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