The Ocular Pathology of Terson’sSyndrome

Fang Ko, MD, David L. Knox, MD

Purpose: To improve understanding of vision loss and clinical findings, we studied gross and microscopicpathology of retinas and optic nerves of individuals with Terson’s syndrome.

Design: Retrospective case series with clinicopathologic correlation.Participants: We included 109 deceased individuals with Terson’s syndrome.Methods: Histologic sections and gross photographs from 109 cases of Terson’s Syndrome, accessed from

1955 to 1992 at the Wm R. Green Laboratory of Ocular Pathology, were studied and photographed; arepresentative case is described in detail.

Main Outcome Measures: Abnormalities in retina and optic nerve.Results: Hemorrhages occur in vitreous, subhyaloid, sub-internal limiting membrane (ILM), intraretinal,

and subretinal spaces, in association with macular holes, retinal detachments, and optic neuropathy.Subhyaloid hemorrhages have diffuse morphology, whereas sub-ILM are well-demarcated. Continuous andnoncontinuous blood occurs along optic nerves, within nerve sheaths, and in the subdural and subarachnoidspaces.

Conclusions: Blood occurring in various layers and locations of the retina, particularly the macula, causesvarious complications that influence clinical management and visual outcome. Morphology differentiates sub-hyaloid from sub-ILM hemorrhage. Patterns of hemorrhages of optic nerve contribute to understanding mech-anisms of Terson’s syndrome.

Financial Disclosure(s): The authors have no proprietary or commercial interest in any of the materialsdiscussed in this article. Ophthalmology 2010;117:1423–1429 © 2010 by the American Academy of Ophthalmology.

Terson first reported associations between intracranial hem-orrhage and vitreous hemorrhage in 1900.1 Since then,Terson’s syndrome has been defined as vitreous or retinalhemorrhage in the presence of intracranial hemorrhage,occurring in 12.5% to 40% of individuals.2– 6 It is be-lieved that ruptured intracranial aneurysm or head traumarapidly increases the intracranial pressure.3,5 This pres-sure is transmitted through the optic nerve sheath andveins to the optic nerve head and retina, causing ruptureof thin capillary walls.3,5

Reported complications of Terson’s syndrome include vi-sual loss,7 macular holes,8 epiretinal membrane formation,9,10

retinal folds,10,11 proliferative vitreoretinopathy,12,13 and reti-nal detachment.13 It has been suggested that these complica-tions are the result of proliferation of glial and retinal pigmentepithelial elements capable of causing retinal distortion andfibrotic adhesions.8

Reports of the pathology of eyes with Terson’s syndromeare limited. Some reports describe epiretinal membranes.14

Others show blood dissecting between the internal limitingmembrane (ILM) and underlying Müller cell end plates.15

One case report demonstrated preretinal, sub-ILM, intrareti-nal, and optic nerve sheath hemorrhage.16 The present re-port describes 1 representative case, analyzes 30 selected

eyes from 16 individuals, and presents photographs of char-

© 2010 by the American Academy of OphthalmologyPublished by Elsevier Inc.

acteristic pathology seen in the vitreous, retina, and opticnerves of eyes with Terson’s syndrome.

Materials and Methods

Indices of histopathology and photographic collections of casesdiagnosed as “Terson’s syndrome” in the Wm R. Green Labora-tory of Ocular Pathology were searched, retrieved, studied, andselected as emblematic of common features.

Thirty-nine cases were based on autopsies from The JohnsHopkins Hospital, Hopkins Bayview Hospital, or Greater Bal-timore Medical Center. Fifty-eight cases were acquired fromMaryland, Florida, Washington, Delaware, West Virginia, orinternational Eye Banks. Histologic sections were stained withhematoxylin and eosin or Verhoeff-Van Gieson. Twelve caseswere based on histopathologic sections prepared by RichardLindenberg, MD, a neuropathologist at the Maryland MedicalExaminers Office, who donated his collection of ocular tissuesto the Wm R. Green Laboratory. These sections were preparedby unroofing optic canals to study long sections of wholenerves, stained with iron stain or Verhoeff-Van Gieson.

The location and severity of tissue deposition of blood was thedefining characteristic in this study. The eyes of all individualswere classified as either trauma or primary intracranial hemorrhageand their ages tabulated (Fig 1).

Informed consent was not required because individuals were

deceased. This work is compliant with Health Insurance Portability

1423ISSN 0161-6420/10/$–see front matterdoi:10.1016/j.ophtha.2009.11.028

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Ophthalmology Volume 117, Number 7, July 2010

and Accountability Act; all possible individual identifiers havebeen removed. Institutional Review Board of The Johns HopkinsMedical Institutions, Baltimore, Maryland, decided approval wasnot required for this study. This research adhered to the tenets ofthe Declaration of Helsinki.

Results

Individuals ranged from 3 months to 90 years old, with a meanage of 47.3 years among all individuals, 28.3 years amongtrauma-related cases, and 56.1 years among those with vas-culogenic intracranial hemorrhage. Of the 4 individuals �5years old, 3 died in motor vehicle accidents and 1 died ofintracranial hemorrhage of unknown etiology. Figure 1 shows

™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™Figure 2. Right eye of patient 14. Hemorrhage in the outer plexiform la�4). GCL � ganglion cell layer; ILM � internal limiting membrane; IPL

Figure 3. Left eye of patient 14. A, Gross photo of dome-shaped, dense,in cross section beneath the internal limiting membrane (ILM; arrowheaoriginal magnification, �10). C and D, Origins of detached ILM from an

Figure 4. Vitreous, subhyaloid, and sub-internal limiting membrane (ILM)hematoxylin and eosin; original magnification, �20). B, Subhyaloid (thganglion cell, bipolar cell, and outer plexiform layers (stain: hematoxyhemorrhage with diffuse appearance and irregular border.

Figure 5. Retinal hemorrhages. A, Retinal hemorrhages in bipolar cell aeosin; original magnification, �4). B, Blood in anterior retina, ganglion celmagnification, �10). C, Distended retinal veins in an eye with hemorrhabipolar cell, and OPL (stain: hematoxylin and eosin; original magnificatioinner plexiform layer; ONL � outer nuclear layer; R&C � rods and con

Figure 6. Macular hemorrhage. Macula has hemorrhage in outer plexifmagnification, �10). GCL � ganglion cell layer; ILM � internal limitingrods and cones.

Figure 7. Macular hole. Macular hole with hemorrhage in subhyaloid spsubretinal space (stain: hematoxylin and eosin; original magnification, �4

Figure 1. Age distribution of patients. The 109 patients ranged from 3months to 90 years old, with a mean of 47.3 years, median of 51.0 years,and standard deviation (SD) of 21.2 years. The mean age among patientswith trauma-related Terson’s syndrome was 28.3 years old (median, 23.5;SD, 22.6), and the mean among with intracranial hemorrhage as theinciting event was 56.1 years (median, 57.0; SD, 13.8). Data were notavailable (NA) for 6 patients.

plexiform layer; ONL � outer nuclear layer; R&C � rods and cones.

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age distribution of the 109 individuals studied, where Terson’ssyndrome was caused by trauma, intracranial hemorrhage, orunknown.

Thirty eyes from 16 individuals were randomly selected from109 cases to be specially examined microscopically. Table 1describes the age, gender, cause of death, estimated number ofdays between onset of Terson’s syndrome and death, and timebetween death and autopsy. Ten of the 16 individuals were female.Causes of death include trauma (fall, motor vehicle accident,gunshot) or subarachnoid hemorrhage from ruptured intracranialaneurysm or hypertension. All cases involved intracranial hemor-rhage. One case (Table 1, number 13) was notable for Marfan’ssyndrome. Ten individuals died within 2 days of onset of Terson’ssyndrome, 3 individuals died after 3 to 5 days of onset, and in 3,the duration was unknown.

The following representative case (Table 1, number 14) isdescribed. A 40-year-old woman with a history of hypertensionpresented with sudden onset headache on March 5, 1997. Com-puted tomography at that time was unremarkable. Over theensuing 2 months, she experienced intermittent headaches. OnMay 3, 1997, she noticed dizziness with her headaches. On May10, 1997, she was found unresponsive at home. Repeat com-puted tomography revealed an intraparenchymal hematoma ofthe left frontal lobe and hemorrhage into the left lateral ventri-cle; no significant midline shift or herniation was noted. Afterprogressive worsening of her Glasgow Coma Score, an intra-ventricular catheter was placed. Subarachnoid hemorrhage withassociated cerebral edema caused mass effect and uncal herni-ation. The individual rapidly developed progressive encepha-lopathy and died on May 11, 1997. In hospital, it was observedthat the right pupil did not react to direct stimulation. Ocularfundoscopy was not reported.

Postmortem examination on May 12, 1997, revealed a 7-mmberry aneurysm of the left anterior communicating artery withassociated hematoma, subarachnoid hemorrhage, and extensivecerebral edema. The left frontal cortex contained a 2.5-cm hema-toma. There was diffuse subarachnoid hemorrhage. The mid-

™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3PL) of the retina (stain: hematoxylin and eosin, original magnification,

ner plexiform layer; ONL � outer nuclear layer; R&C � rods and cones.

ly edged hemorrhage. B, Histopathology of the dome-shaped hemorrhageith hemorrhage in anterior retina (arrow; stain: hematoxylin and eosin;r retina (stain: hematoxylin and eosin; original magnification, �20).

orrhages. A, Vitreous (arrow) and sub-ILM hemorrhage (arrowhead; stain:ow) and sub-ILM hemorrhage (arrowhead), with retinal hemorrhages innd eosin; original magnification, �10). C, Gross photo of subhyaloid

ter plexiform layers (OPL), and rods and cones (stain: hematoxylin andolar cell, OPL, and subretinal space (stain: hematoxylin and eosin; originalsub-ILM (ILM is detached and not visible in this image), ganglion cell,0x). GCL � ganglion cell layer; ILM � internal limiting membrane; IPL �

ayer (OPL), and rods and cones (stain: hematoxylin and eosin; originalrane; IPL � inner plexiform layer; ONL � outer nuclear layer; R&C �

anglion cell layer, inner nuclear layer, outer plexiform layer (OPL), andL � ganglion cell layer; ILM � internal limiting membrane; IPL � inner

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Ko and Knox � Ocular Pathology of Terson’s Syndrome

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Ophthalmology Volume 117, Number 7, July 2010

brain, pons, and ventricular system showed diffuse, small areas ofhemorrhage.

Grossly, the right eye showed subconjunctival hemorrhage(4 � 2 mm) at the superotemporal limbus and 3 well-demarcated,dome-shaped peripapillary retinal hemorrhages (1.0–1.5 mm indiameter). No vitreous hemorrhage was noted. Microscopic exam-ination revealed 2 areas of hemorrhage in the outer plexiform layer(OPL), one in the temporal aspect of the macula, the other 1.5 mmanterior to the optic nerve. Figure 2 demonstrates outer plexiformmacular hemorrhage. The optic nerve was remarkable for crushartifact. Additional hemorrhages were seen in the subarachnoidspace, the subdural space, and within the dural sheath of the opticnerve.

The left eye grossly showed subconjunctival hemorrhage(4.0 � 2.5 mm) at the temporal limbus, a dome-shaped sub-ILMhemorrhage with raised edges inferior and temporal to the opticdisc (Fig 3A), and a retinal hemorrhage (1 mm in diameter)inferior and nasal to the optic disc. Microscopically, a large hem-orrhage (9 mm in diameter) was present beneath ILM at themacula. Hemorrhage was also detected in the inner nuclear layer,OPL, and beneath the retina. Figures 3B–D demonstrate hemor-rhages beneath the ILM, elevation of adjacent ILM, points of

™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™Figure 8. Crush artifact and optic nerve hemorrhage. Optic nerve in cross sectiomagnification, �3) and (B) hemorrhage within the optic nerve sheath, subdural sp

Figure 9. Optic nerve hemorrhage. Optic nerve hemorrhages in cross sect�4); (B and C) in subdural and subarachnoid space with varying levelSubarachnoid hemorrhage in longitudinal section of optic nerve (stain: h

Figure 10. Two types of optic nerve hemorrhage. (A) Multifocal discretehigher magnification of distended retinal veins in the same eye (stain: iro

Table 1. Clinical Setting of 1

Case Age/Gender Cause of Death

1 90/Female Fall, subdural hematoma2 69/Female Intracranial bleeding3 26/Male Subarachnoid hemorrhage, cardiac arrest4 7/Female MVA5 25/Male Gunshot wound to head6 41/Male Cerebral hemorrhage7 62/Female CVA8 53/Female Subarachnoid hemorrhage9 64/Female Seizures and hydrocephalus secondary to rup

intracranial aneurysm10 68/Female Subarachnoid hemorrhage (history of HTN,

of emesis, collapsed, and pronounced brainarrival to hospital)

11 34/Female Subarachnoid and intracranial hemorrhage12 64/Male Massive cerebral bleed (patient was well unt

found him prone on bathroom floor)13 37/Female Subarachnoid hemorrhage of posterior fossa,

hemorrhage of spinal cord, Marfan syndro14 40/Female Ruptured berry aneurysm of left anterior com

cerebral artery15 60/Male Refractory intracranial bleed16 64/Male Intracranial hemorrhage of right cerebral he

with rupture through

CVA � cerebral vascular accident; HA � headache; HTN � hypertens

(stain: Verhoeff-Van Gieson; original magnification, �1) with optic chiasm (a

1426

detachment of ILM from anterior retina, and compression of theretina with attenuation of the thickness of the outer nuclear celllayer. The optic nerve showed subdural hemorrhage extending intothe inner 50% of the dural sheath.

The range of pathology observed among the 30 specificallystudied eyes is summarized in Table 2 (available online athttp://aajournal.org). Vitreous hemorrhage was present in 11eyes (Fig 4A) and diffuse subhyaloid hemorrhage was presentin 10 eyes (Fig 4B). Intraretinal hemorrhage was present in alleyes: 23 eyes had well-demarcated, dome-shaped hemorrhagebeneath the ILM (Fig 4B–C), 16 eyes had blood in the ganglioncell layer (Fig 5), 19 eyes had hemorrhage in bipolar cell layer (Fig5), 20 eyes had hemorrhage in the OPL (Fig 5), 9 eyes had hemor-rhage in outer nuclear layer (Fig 6), and 4 eyes had hemorrhage of therods and cones (Figs 6 and 7). Subretinal hemorrhage was seen in 14eyes (Figs 5B and 7). Figure 7 demonstrates infiltration, distension,and rupture of the macula from an individual who died within 2 daysof intracranial hemorrhage. Notably, no eyes had hemorrhage in theinner plexiform layer (IPL).

The range of histopathology apparent in optic nerves issummarized in Table 3 (available online at http://aajournal.org).A crush artifact (Fig 8) was seen in the optic nerves of 14 eyes.

™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3h (A) diffuse distribution of crush artifact (stain: hematoxylin and eosin; originalnd subarachnoid space (stain: hematoxylin and eosin; original magnification, �3).

) in subdural space (stain: hematoxylin and eosin; original magnification,ensity (stain: hematoxylin and eosin; original magnification, �20). D,

oxylin and eosin; original magnification, �3).

nerve hemorrhage (stain: iron stain; original magnification, �1) with (B)in; original magnification, �10). C, Continuous optic nerve hemorrhage

ients with Terson’s Syndrome

Estimated No. of Days fromOnset of Terson’s until Death

Time between Deathand Autopsy (hours)

2 22.52 1.5

N/A 21 171 8.51 2

N/A 1N/A 1.5

1 2.5

n onsetupon

Same day 0.5

3 2wife 1 8

dural 4 �24

icating 1 �24

5 5.5ere 1 15

VA � motor vehicle accident; N/A � not available.

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Hemorrhage was present in the dural sheaths of 9 eyes, in thesubdural spaces of 19 eyes, in the subarachnoid spaces of 20eyes, and within the pia mater of 2 eyes (Fig 9). Figure 10A–Cfrom the Lindenberg collection shows optic nerve hemorrhagesfrom 2 individuals who died after trauma. Figure 10A demon-strates focal dural and subdural hemorrhage in midorbital opticnerve, with no evidence of extensions from intracranial bloodalong optic nerve canal. Distended anterior retinal veins can beseen in this eye (Fig 10B). Figure 10C demonstrates severesubdural blood from the optic chiasm, along the optic canal, tothe optic nerve scleral junction.

Discussion

Terson’s syndrome has been reported to cause epiretinalmembranes, retinal folds, proliferative vitreoretinopathy,retinal detachment, and macular holes.8 –13 Our his-topathologic analysis was undertaken to increase under-standing of mechanisms which threaten vision. As shownin Figure 1, our study found a wide range of individualages. The elderly mainly died of vasculogenic intracra-nial hemorrhages; younger individuals largely died oftrauma-related causes.

Vitreous hemorrhage (Fig 4A) in the visual axis ob-viously reduces visual acuity. Figure 4B demonstrates athin layer of hemorrhage overlying retina. Yokoi et al9

proposed that vitreous hemorrhage breaks down the ILM,causing glial cell migration and proliferation into thevitreous cavity and epiretinal membrane formation.9 Thispossibility provides an argument for early, operative re-moval of blood.

Previous authors have attempted to distinguish be-tween subhyaloid and sub-ILM hemorrhages.15,17 Wefound that subhyaloid hemorrhages are diffuse, irregu-larly edged, and vary in density (Fig 4C), whereas sub-ILM hematomas are well-demarcated and dome shaped(Fig 3A, B).

Both subhyaloid and sub-ILM hemorrhages can bepresent in the same area (Fig 4B). This corroborates apreviously reported “double ring” sign caused by con-current subhyaloid and sub-ILM hemorrhage.18 Fig-ures 3C–D show points at which ILM detaches fromunderlying retina. Hematoma beneath the ILM can causeelevation of the membrane, explaining the “macularring”18 reported by Sadeh et al19; as the sub-ILMhemorrhage contracts and serum is absorbed, the remain-ing ILM wrinkles and is seen as a folded, reflectivesurface.

Blood may elevate retina, causing retinal folds, pro-liferative vitreoretinopathy, and retinal detachment (Figs5 and 6). In some individuals, decreased visual acuitypersists after surgery.4,20,21 Blood at various layers of theretina (Fig 5), particularly at the macula (Fig 6), mayexplain the long-term loss of visual acuity.

Although hemorrhage was seen throughout the retina andsubretinal space, it was not found in the IPL of any eye (Figs2A, 3B, C, 4B, 5, 6 and 7). Even when there was massivehemorrhage throughout the retina, the IPL was spared. Thisimplies that the IPL is a layer of decreased vascularity and

vulnerability.

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Disruption of retina by hemorrhage caused macularhole in an individual who died within 2 days of onset ofTerson’s syndrome (Fig 7). There was no apparent vit-reoretinal traction, the prevailing mechanism proposedby Gass.22 In this case, there was no clinical informationof prior macular disease. The obvious traumatic disrup-tion of the retina is consistent with blood dissecting fromruptured vessels and entering the retinal layers and sub-retinal space to weaken and disrupt the macula, resultingin a macular hole. Development of a hemorrhage-inducedmacular hole within 2 days argues for early evaluation ofthe retina in clinically stable individuals.

Hemorrhage of the optic nerve sheath is a frequentcomplication of Terson’s syndrome23; in this study, itoccurred within the dural sheath, subdural space, sub-arachnoid space, or pia mater (Fig 9). Figure 10A dem-onstrates multifocal optic nerve hemorrhages. In 1943,Ballantyne24 proposed and presented evidence that in-traocular and subdural optic nerve hemorrhages of Ter-son’s syndrome were locally multifocal and not exten-sions of intracranial blood. According to this explanation,multiple foci of hemorrhage can cause continuous bloodalong optic nerve canal from chiasm to sclera (Fig 10B).Although it is possible that there are 2 mechanisms forTerson’s syndrome, we believe multifocal bleeding is themost common.

This study is limited in that eyes used for histopatho-logic analysis were necessarily acquired from deceasedindividuals, possibly describing a range of disease that ismore severe than what is usually seen clinically. Futurestudies could determine whether the range of histopatho-logic findings correlates with severity of disease by in-corporating orbital ultrasound, ocular coherence tomo-graphy, and magnetic resonance imaging. From thisstudy, we see a need for clinicians to be more aggressivein early evaluation of individuals with head traumaand subarachnoid hemorrhage from ruptured intracranialvessels.

Current recommendations in literature suggest 3 to 6months of observation after the acute event, followed byvitrectomy if there is no improvement in visual acu-ity.6,25–28 This report demonstrates a range of pathologythat occurs within 1 week of onset of Terson’s syndrome,including vision-threatening findings of vitreous hemor-rhage, retinal hemorrhage, foveal damage, and macularhole. Our study suggests that earlier definition of theextent and location of bleeding, before 3 months, canoptimize clinical management. Although it is not possibleto obtain histopathology without damaging eyes of livingindividuals, ultrasound, magnetic resonance imaging, andocular coherence tomography can bridge the gap betweenclinical and pathologic findings. These diagnostic stud-ies, together with knowledge of the range of disease thatoccurs in Terson’s syndrome demonstrated by our study,may guide clinicians in determining whether earlier sur-gery may improve clinical outcomes of visual acuity and

rehabilitation.

Ko and Knox � Ocular Pathology of Terson’s Syndrome

References

1. Terson A. De l’hemorrhagie dans le corps vitre au cours del’hemorrhagie cerebrale. Clin Ophthalmol 1900;6:309–12.

2. Ness T, Janknecht P, Berghorn C. Frequency of ocular hem-orrhages in patients with subarachnoidal hemorrhage. GraefesArch Clin Exp Ophthalmol 2005;243:859–62.

3. Medele RJ, Stummer W, Mueller AJ, et al. Terson’s syndromein subarachnoid hemorrhage and severe brain injury accom-panied by acutely raised intracranial pressure. J Neurosurg1998;88:851–4.

4. Kuhn F, Morris R, Witherspoon CD, Mester V. Tersonsyndrome: results of vitrectomy and the significance of vitre-ous hemorrhage in patients with subarachnoid hemorrhage.Ophthalmology 1998;105:472–7.

5. Pfausler B, Belcl R, Metzler R, et al. Terson’s syndrome inspontaneous subarachnoid hemorrhage: a prospective study in60 consecutive patients. J Neurosurg 1996;85:392–4.

6. Fountas KN, Kapsalaki EZ, Lee GP, et al. Terson hemorrhagein individuals suffering aneurysmal subarachnoid hemorrhage:predisposing factors and prognostic significance. J Neurosurg2008;109:439–44.

7. McCarron MO, Alberts MJ, McCarron P. A systematic reviewof Terson’s syndrome: frequency and prognosis after subreti-nal haemorrhage. J Neurol Neurosurg Psychiatry 2004;75:491–3.

8. Rubowitz A, Desai U. Nontraumatic macular holes associatedwith Terson syndrome. Retina 2006;26:230–2.

9. Yokoi M, Kase M, Hyodo T, et al. Epiretinal membraneformation in Terson syndrome. Jpn J Ophthalmol 1997;41:168–73.

10. Sharma T, Gopal L, Biswas J, et al. Results of vitrectomyin Terson syndrome. Ophthalmic Surg Lasers 2002;33:195–9.

11. Keithahn MA, Bennett SR, Cameron D, Mieler WF. Retinalfolds in Terson syndrome. Ophthalmology 1993;100:1187–90.

12. Ritland JS, Syrdalen P, Eide N, et al. Outcome of vitrectomyin patients with Terson syndrome. Acta Ophthalmol Scand2002;80:172–5.

13. Velikay M, Datlinger P, Stolba U, et al. Retinal detachmentwith severe proliferative vitreoretinopathy in Terson syn-

drome. Ophthalmology 1994;101:35–7.

Medicine, Baltimore Maryland.

14. Garcia-Arumi J, Corcostegui B, Tallada N, Salvador F.Epiretinal membranes in Terson’s syndrome: a clinicopatho-logic study. Retina 1994;14:351–5.

15. Friedman SM, Margo CE. Bilateral subinternal limiting mem-brane hemorrhage with Terson syndrome. Am J Ophthalmol1997;124:850–1.

16. Morris DA, Henkind P. Relationship of intracranial, optic-nerve sheath, and retinal hemorrhage. Am J Ophthalmol 1967;64:853–9.

17. Weingeist TA, Goldman EJ, Folk JC, et al. Terson’ssyndrome: clinicopathologic correlations. Ophthalmology1986;93:1435–42.

18. Srinivasan S, Kyle G. Subinternal limiting membrane andsubhyaloid haemorrhage in Terson syndrome: the macular’double ring’ sign [letter]. Eye 2006;20:1099–101.

19. Sadeh AD, Lazar M, Loewenstein A. Macular ring in a patientwith Terson’s syndrome. Acta Ophthalmol Scand 1999;77:599–600.

20. Garweg JG, Koerner F. Outcome indicators for vitrectomy inTerson syndrome. Acta Ophthalmol 2009;87:222–6.

21. Schultz PN, Sobol WM, Weingeist TA. Long-term visualoutcome in Terson syndrome. Ophthalmology 1991;98:1814–9.

22. Gass JD. Idiopathic senile macular hole: its early stages andpathogenesis. Arch Ophthalmol 1988;106:629–39.

23. Gauntt CD, Sherry RG, Kannan C. Terson syndrome withbilateral optic nerve sheath hemorrhage. J Neuroophthalmol2007;27:193–4.

24. Ballantyne AJ. The ocular manifestations of spontaneous sub-arachnoid haemorrhage. Br J Ophthalmol 1943;27:383–414.

25. Augsten R, Königsdörffer E. Terson syndrome—a contribu-tion to the timing of operation for pars plana vitrectomy [inGerman]. Klin Monatsbl Augenheilkd 2007;224:674–7.

26. Biousse V, Mendicino ME, Simon DJ, Newman NJ. Theophthalmology of intracranial vascular abnormalities. Am JOphthalmol 1998;125:527–44.

27. Garfinkle AM, Danys IR, Nicolle DA, et al. Terson’ssyndrome: a reversible cause of blindness following subarach-noid hemorrhage. J Neurosurg 1992;76:766–71.

28. Vanderlinden RG, Chisholm LD. Vitreous hemorrhages andsudden increased intracranial pressure. J Neurosurg 1974;41:

167–76.

Footnotes and Financial Disclosures

Originally received: April 22, 2009.Final revision: November 18, 2009.Accepted: November 18, 2009.Available online: March 29, 2010. Manuscript no. 2009-556.

From The Wilmer Eye Institute, The Johns Hopkins University School of

Financial Disclosure(s):The authors have no proprietary or commercial interest in any of thematerials discussed in this article.

Correspondence:David L. Knox, MD, The Johns Hopkins Hospital, Woods 275, 601 N

Broadway, Baltimore MD 21287-9013. E-mail: daknox@jhmi.edu.

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Table 2. Hemorrhage in the Vitreo

Case/EyeVitreous

HemorrhageSubhyaloidHemorrhage Sub-ILM GCL

1 OD — — � —1 OS � — � —2 OD — � � �2 OS — — � �3 OD — � — �3 OS � � � �4 OD — — � �4 OS — — — —5 OD � — � �5 OS � � � �6 OD — — � —6 OS — � � —7 OD — — � �8 OD � � � �8 OS � � � �9 OS � — � �10 OD — — — �10 OS — — — —11 OD � — � �11 OS — — � �12 OD — — � —12 OS — — — —13 OD — — � �13 OS — — � �14 OD � — � —14 OS � — � —15 OD — — � —15 OS — � � —16 OD � � — —16 OS — � — —

GCL � ganglion cell layer; ILM � internal limiting membrane; IPL � inplexiform layer; OS � left eye.

us Cavity, Retina, and Subretinal Space

Intraretinal Hemorrhage SubretinalHemorrhageIPL INL OPL ONL Rods and Cones

— — — — — —— — — — — —— � � � — �— � � — — �— � — — — —— � � — — —— — � — — —— — — — — —— � � — � —— � � — — �— — — — — �— — — — — —— � � � — �— � � � — �— � � � — �— � � � � �— — — — — �— — � — — —— � � � — �— � � � — �— � � — — —— � � — — —— � � � � �— � — — — —— � � — — —— � � — — �— — � — — —— — — — — �— � � — � —— — — � — —

ner plexiform layer; OD � right eye; ONL � outer nuclear layer; OPL � outer

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Ko and Knox � Ocular Pathology of Terson’s Syndrome

Table 3. Histopathology of the Optic Nerve

Case/EyeCrush

ArtifactIntrasheathHemorrhage

SubduralHemorrhage

SubarachnoidHemorrhage

Hemorrhage withinPia Mater

1 OD � — � � �1 OS � � � � —2 OD — — � � —2 OS — — � � —3 OD — — — � —3 OS � — — — —4 OD — — — — —4 OS — — — — —5 OD � � � � —5 OS � � � � —6 OD � — — — —6 OS � — � — —7 OD — � � � —8 OD � — � � —8 OS — � � � —9 OS N/A — � � —10 OD — — � � —10 OS — � � � �11 OD � — — — —11 OS � — — — —12 OD — — � � —12 OS — — � � —13 OD � — — � —13 OS � — — — —14 OD � � � � —14 OS — � � — —15 OD — — — — —15 OS — � � � —16 OD � — — � —16 OS — — — � —

N/A � cross-section is not available; OD � right eye; OS � left eye.

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