Spontaneous intrapapillary hemorrhage with adjacent peripapillary subretinal hemorrhage in adolescents

Abstract

Purpose: The purpose of this study was to report the clinical features of seven eyes of seven adolescent patients with spontaneous intrapapillary hemorrhage with adjacent peripapillary subretinal hemorrhage (IHAPSH).

Design: This was a retrospective case series study.

Participants: A total of seven adolescent patients with IHAPSH were participated.

Methods: All the patients were seen at the Joint Shantou International Eye Centre, between 2006 and 2014. The patient demographics, clinical history, vision, fundoscopy, and results of relevant investigations were collected.

Main Outcome Measures: This was a clinical history and fundoscopic appearance.

Results: All eyes (four males and three females) with IHAPSH had a median age at presentation of 15 years (mean 14.7, range 11-19). Four cases presented in the right eye and three cases in the left eye. All seven patients presented with blurring of vision and floaters upon awakening in the morning. No obvious underlying causes or predisposing factors were present. The presenting visual acuity ranged from 0.12 to 1.00. One eye had no refractive errors and the remaining six eyes had myopia ranging mild to moderate (-0.25 diopters (D)--4.00 D). None had tilted discs. In four eyes, subretinal hemorrhage was < 2 disc diameters. There was associated vitreous hemorrhage in five eyes. There were no posterior vitreous detachments in any of the eyes. Visual field test showed an enlarged blind spot in four cases. Optical coherence tomography of the disc revealed optic disc swelling in two cases. Fluorescein angiography demonstrated leakage in the late phase of three eyes. At 2-24 months follow-up, the hemorrhageresolved in all seven cases with vision recovering fully to 20/20. Visual field defect of enlarged blind spots improved with the resolution of intrapapillary and subretinal hemorrhages.

Conclusions: The condition of IHAPSH resolved spontaneously without intervention in all cases. There appeared to be no predisposing factors for the development of this condition. Previously reported risk factors such as myopia, a tilted disc, Valsalva maneuver, and posterior vitreous detachment were not seen in these cases. This is the 1st time a series of young adults have been reported with this condition, all of whom presented in the same manner and had the same clinical outcomes.

Introduction

A clinical syndrome of intrapapillary hemorrhage with adjacent peripapillary subretinal hemorrhage (IHAPSH) was first described in 1975.^[1] These cases were distinct due to the significant bleeding within the optic disc that extends into the peripapillary subretinal space; in some cases, vitreous hemorrhageoccurs too. It has been described more frequently in patients with myopia, small, mildly dysplastic, tilted optic discs^[2-8] and in the young Asian population.^[3-5,8] Despite the alarming appearance, a good visual prognosis has been documented where there is spontaneous resolution without intervention.^[1-8] The cause of this condition is unknown. Vitreous traction on the optic disc during posterior vitreous detachment has been proposed as onepossible cause for IHAPSH.^[1-3,6] It has also been recognizedas a subtype and consequence of Valsalva retinopathy.^[5,6]The purpose of this study was to describe further the clinicalcharacteristics associated with IHAPSH in adolescent Chinese.

Materials and Methods

Seven patients with IHAPSH who presented to Joint ShantouInternational Eye Centre in Shantou, China, between January2006 and December 2014 were identified. Data were collectedand evaluated retrospectively in this observational case series.The local ethical review board approved this study and informedconsent was obtained from all patients.

Only those patients with acute bleeding within the optic discand adjacent peripapillary subretinal hemorrhage surroundingthe disc hemorrhage at presentation, as visualized withophthalmoscopic evidence, were included. Those patients withhemorrhage at the optic disc only were not included. All patientswith secondary causes for disc hemorrhage were excluded fromour study, which include, bleeding diathesis, Terson's syndrome,peripapillary subretinal neovascularization, ischemic opticneuropathy, polypoidal choroidal vasculopathy, and Leber'sidiopathic stellate neuroretinitis.

All seven patients included in the study had demographic datacollected, refractive error recorded, and history of presentingcomplaint with possible precipitating events reviewed. Allpatients underwent best-corrected visual acuity, pupillaryresponses, and slit-lamp biomicroscopic examination.

Fundus photography was performed for all eyes. Thisincluded descriptions of disc anatomy, clarity of disc margins,multilayer hemorrhage location and extent, measured in discdiameters, and retinal features in the involved and felloweye. Selected cases had further diagnostic testing. Five of thepatients had fluorescein angiography done, optical coherencetomography (OCT) of the disc was performed for two cases, andB-scan ultrasonography was performed for one case. Finally, aHumphrey visual field assessment was done for four cases.

All patients were followed up until complete resolution ofthe hemorrhage and vision had fully recovered. The follow-upperiod ranged from 2 to 24 months with a mean of 10.5 months.

Results

All seven patients were adolescents with a median age atpresentation of 15 years (mean 14.7, range 11-19). All patientswere of Chinese ethnicity. There were three female andfour male patients. All patients presented with unilateral eyeinvolvement (four in the right eye and three in the left eye). Themean refractive error was -1.19 D with six mild to moderatelymyopic eyes (range from -0.25 D to -4.00 D). Using thedefinition of mild myopia as < 3 D, moderate myopia 3-6 D, andsevere myopia of >6 D, one patient had no refractive error, fourhad mild myopia, and two had moderate myopia. No patienthad high myopia. They had no significant ocular or medicalhistory. There was no preceding history of straining or Valsalvamaneuvers. All patients presented with similar symptoms,namely, blurring of vision and floaters in the involved eye onawakening in the morning. The presenting best-corrected visualacuity ranged from 0.12 to 1.00. Intrapapillary hemorrhage wasobserved nasally in two eyes and in 360° in one eye. Five patientshad associated vitreous hemorrhage, in which two patients had amild form of vitreous hemorrhage and three had severe vitreoushemorrhage that obscured further ancillary investigations. Theadjacent subretinal hemorrhage was on the nasal side of the discin all eyes in this series. Severe subretinal hemorrhage extendingover two disc diameters was present in four eyes [Figure 1a]. Theremaining three eyes demonstrated mild subretinal hemorrhagewithin one disc diameter in size [Figure 1b]. None of the patientshad a posterior vitreous detachment, complete or incomplete, asdefined by the presence of a visible, freely moving Weiss' ring onfundal biomicroscopy. B-scan ultrasonography was performedin one patient, revealing no evidence of a partially detachedposterior vitreous detachment, vitreopapillary traction. Onepatient was confirmed having bilateral optic disc drusen and wasexcluded from this study.

All eyes revealed blurred disc margins, of which it was mild infive eyes and marked in two eyes. Similarly, blurred disc marginswere seen in the fellow eye in five eyes, with a mild case in foureyes and marked in one eye. None of our patient had an unusualdisc size or configuration and none were tilted.

Spectral-domain OCT (Cirrus HD-OCT; Carl ZeissMeditec, Inc., Dublin, CA) of the optic nerve head and retinalnerve fiber layer was performed in two of seven eyes, at the timeof presentation. They showed a thickened retinal nerve fiberlayer in the nasal sector of the optic disc, which correspondedto the area of disc hemorrhage. In both eyes, a crowded disc wasalso demonstrated. No optic disc tilting presents. Furthermore,no bleeding occurred at the macula and the OCT scans of themacula were, therefore, normal.

We performed fundus fluorescein angiography (FFA) in fiveeyes. In early phase FFA, there was masking of fluorescein by thedisc and subretinal hemorrhage at the respective area [Figure 2].Late phase FFA showed fluorescein leakage in only two cases.

Visual field testing, using a full-threshold 24-2 Swedishinteractive thresholding algorithm Humphrey field analyzer(Carl Zeiss Meditec, Inc., Dublin, CA), was performed in fourof seven eyes. They all, acutely, showed an enlarged blind spot.The area of enlarged blind spot increased with the size andextent of subretinal hemorrhages. Three patients underwentmagnetic resonance imaging (MRI) brain, without Gadoliniumenhancement, which was reported as normal. These patients hadan MRI brain to rule out other differential etiology, primarilyto look for causes of intracranial hypertension that may lead topapilledema and disc hemorrhage.

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All disc and adjacent subretinal hemorrhages resolvedover a period of 1-9 months (mean of 3.5 months). Once thehemorrhages resolved the visual acuity recovered to 20/20 inall eyes and the visual field defect of enlarged blind spot alsoreduced in size.

Discussion

IHAPSH is a rare benign clinical syndrome with excellentprognosis, characterized by a sudden deterioration of visionand hemorrhage in and surrounding the optic nerve head. Theprevious reports on IHAPSH described patients from a diverserange of age and ethnicities.^[1-3] In this case series, findingswere consistent with the previous reports in some respects butdissimilar in several key aspects, which will be discussed in thefollowing passages.

First, the coexistence of a crowded, tilted disc,^[2,5,6,8] discedema,^[2,5] and high myopia^[9,10] has been observed in previouslypublished reports. Our series show similar results as crowdedand edematous optic nerve head was found on fundoscopicexamination and was further supported by similar findings onOCT in the cases this was performed in. This is in keeping withthe notion that patients with a crowded optic nerve head arepredisposed to IHAPSH. A structurally unique vascular anatomyof the prelaminar portion of the disc has been documented.^[11,12]This region is supplied by the peripapillary choroid and posteriorshort ciliary arteries and most of the venous drainage is tothe central retinal vein with the remaining drainage to theperipapillary choroidal veins. Since myopic, tilted, discs havean elevated superior and nasal margin, it has been suggestedby Kokame^[5] that this leaves capillaries vulnerable to bleedingwhen retinal and choroidal tissues are dragged over and aroundthe elevated edge.

Teng et al.^[8] proposed an additional theory that small scleralcanal compression could play a major role in the pathogenesisof IHAPSH. They observed on OCT that nerve fibers reachthe nasal retina by entering through a small scleral ring with asharp nasal edge, along an acutely angled pathway, whereastemporal fibers gently bend over a rounded scleral margin.Thus, predisposing the choroidal arteries of the prelaminar nasalrim portion to vascular compromise and bleeding. It has beenreported that increased myopia is associated with increasingtilting of the disc.^[10] However, one aspect of our results wascontrary to previously published suggestion that this conditionis predominantly in patients with high myopia or tilted disc, asexemplified when none of our seven cases had tilted discs orhigh myopia. It can be inferred that an alternate theory couldexist. An interplay of ocular motor forces, scleral thinning, andvitreopapillary traction acting on a morphologically vulnerableoptic disc has been suggested by Sibony et al.^[7]

It should be noted that this typical appearance can mimicpapilledema which may lead to unnecessary investigations, brainimaging, and a misdiagnosis.^[6] Clinical judgment and cautionare needed to differentiate other causes of disc hemorrhagefrom this benign syndrome with no systemic correlations. Thisis especially important as other conditions have been describedto have hemorrhagic complications. These include opticdisc drusen,^[6,13] bleeding diathesis,^[14] increased intracranialpressure,^[15] peripapillary subretinal neovascularization,^[16] andLeber's idiopathic stellate neuroretinitis.^[5] Knowledge of theseconditions would be helpful on devising the most appropriatemanagement plan.

Furthermore, all our patients with IHAPSH are adolescentswith ages ranging from 11 to 19 and of Chinese origin. Toexemplify the contrast, a case series conducted by Sibony et al.^[7]revealed all 10 of them to be of Caucasian ethnicity with a rangeof 8-63 years of age. A female predominance was noted in somestudies^[4,7] and a male predominance in others.^[8] In keeping witha study of 16 eyes by Hwang and Lin,^[6] we similarly report nogender predominance. It can be inferred that gender differencesmay not be determining factor in the development of this rarecondition.

The etiology of IHAPSH remains largely unknown; asmentioned previously, some believe that it is caused by tractionof the vitreous at the optic disc.^[1-3,6] This was also suggested bySchepens^[17] who postulated that this vitreopapillary tractioncould lead to blurring of disc margins and elevation of the disc,causing tearing of superficial vessels which leads to hemorrhagein and around the optic disc. He described this as the "pseudopapilledema"phenomenon, in which there was incompleteposterior vitreous detachment, due to firm vitreopapillaryattachments, that has yet to be weakened by age proven byanatomic evidence.^[18-20] Katz and Hoyt^[2] supported this theorywhen they found the posterior vitreous body separated from theretina but continued to be attached to the disc based on glial tagson the optic discs and B-scan ultrasonography results. Notably,none of the patients in this study had signs of posterior vitreousdetachment, suggesting that this is an unlikely cause in our groupof patients.

The previous studies also postulated that IHAPSH may beprecipitated by the Valsalva maneuver. This phenomenon wasfirst described in 1973 where there is an elevation of venouspressure due to the rapid rise in intra-abdominal or intrathoracicpressure against a closed glottis, which is transmitted to theeye and results in the rupture of typically, perifoveal capillariesbeneath the internal limiting membrane, in the macular region.^[21] A plethora of Valsalva maneuver-induced retinal hemorrhagehas been documented in literature; these include during amotorcycle ride,^[22] vigorous sexual activity,^[23] while inflatingparty balloons,^[24] weight lifting,^[25] and aerobic exercise.[26]Hence, it has also been suggested that disc and subretinalhemorrhage could be a subtype of Valsalva hemorrhagicretinopathy.^[5,26] Although, the actual location of haemorrhageis variable, that is, subretinal, intraretinal or subhyaloid.^[21]Kokame et al.^[4] described a more direct mechanism where thesudden, shearing, stress causes rupture of susceptible choroidalcapillaries on the nasal rim of the optic nerve head. To furthersupport this hypothesis, it has been recorded on color Dopplerimaging that reduced central retinal artery perfusion occursfollowing sneezing.^[26] However, our study findings refutethis hypothesis as all seven patients in our study suffered fromIHAPSH spontaneously, upon awakening in the morning,without a preceding history of exertion or straining. Thissuggests that, although Valsalva maneuvers can be a precipitantfor IHAPSH, it can also occur without a precipitant, which raisesthe possibility of an alternate explanation.

The key characteristic that distinguishes our series fromthe previous reports is that all our patients presented similarly,namely, a sudden onset of visual blurring after awakening in themorning in one eye. To the best of our knowledge, there wasno mention in literature of the exact timing of visual symptomonset. One factor that could contribute during the night toIHAPSH is the circadian periodicity in blood pressure whichdescribes an extensive lowering of nocturnal levels of bloodpressure, described as a nocturnal dip, with the largest surge onarousal in the morning. This morning peak has been associatedwith an increase in cardiovascular risk and several meta-analyseshave reported the highest prevalence of myocardial infarctionand stroke in the morning hours between 6 am and noon.^[27-29]Another factor could be due to the "non-dipping" pattern ofblood pressure described as being more prevalent in patientswith intracerebral hemorrhage, in which non-dipping is definedas a nocturnal systolic blood pressure dip of < 10%.^[30] Furtherstudies are required to ascertain whether these results can beextrapolated to retinal capillaries.

We acknowledge that the main limitation of this study isits small sample size due to its rarity, which limits our abilityto perform statistical analyses to control for potentiallyconfounding factors.

Conclusions

It is likely that IHAPSH occurs in eyes with an anatomicalpredisposition to some extent, specifically, a crowded andedematous disc. However, the triggering event remains unknownas this study refutes the previous hypothesis that vitreopapillarytraction and Valsalva maneuver at the disc lead to IHAPSH. Itis also presented in both genders in a non-specific manner. Thisis the 1st time a series of young adults have been reported withthis condition, all of whom presented in the same manner onawakening and had the same clinical outcomes.

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