Terson’s SyndromedRate and Surgical Approach in Patients with A Prospective Interdisciplinary Study

Christos Skevas, MD,1,* Patrick Czorlich, MD,2,* Volker Knospe, MD,1 Birthe Stemplewitz, MD,1 Gisbert Richard, MD,1 Manfred Westphal, MD,2 Jan Regelsberger, MD,2 Lars Wagenfeld, MD1

Objectives: To analyze the need for surgical intervention in Terson’s syndrome (TS) and the rate of TS, as well as the effect of pars plana (PPV) with or without internal limiting membrane (ILM) peeling, com- plications, correlations between TS and sex, and the influence of the severity of subarachnoid hemorrhage (SAH) expressed by Glasgow Coma Scale (GCS) score and Hunt and Hess grade on the occurrence of TS. Design: Prospective, uncontrolled, interdisciplinary study. Participants: A total of 102 patients with SAH over a period of 24 months. Methods: Patients were examined on days 1 and 14. A PPV was indicated in cases of nonresorbing (VH). Peeling of the ILM was performed with the help of ILM-BLUE (DORC, Zuidland, The Netherlands) using end-gripping ILM forceps. Main Outcome Measures: Effect of PPV on visual acuity (VA) and timing of intervention in cases of non- resorbing VH. Results: The rate of TS was 19.6% (20/102). The mean age of the patients was 52.111.8 years. Patients presenting with an initial GCS of less than 8 or with high Hunt and Hess grades were more affected by TS. Eight (9 eyes) of the 20 patients with TS (40% of the patients with TS) underwent a PPV for nonclearing vitreous . In 4 patients (4 eyes; 20% of patients with TS), ILM peeling was considered necessary because of sub- ILM bleeding. The mean interval between SAH and PPV was 4.4 months (range, 3e5 months). Postoperative follow-up was 6.4 months. Visual acuity improved in all patients. Best-corrected VAs at first and at last pre- sentations were 2.2 and 0.0625 logarithm of the minimum angle of resolution (logMAR), respectively. For patients who underwent ILM peeling, these values were 1.725 and 0.05 logMAR, respectively. Conclusions: Pars plana vitrectomy and ILM peeling have beneficial effects on the visual rehabilitation of patients with nonclearing VH after TS. We did not identify any safety concerns after PPV in our patients with dense nonclearing hemorrhage that persisted for more than 3 months. 2014;121:1628-1633 ª 2014 by the American Academy of Ophthalmology.

Although Terson’s syndrome (TS) was first described by obstruction of the central retinal vein and choroidal e Litten in 1881,1 it was subsequently named after the French anastomosis6 8 under high intracranial pressure. ophthalmologist Albert Terson in 1900.1 Today, TS is A broad variation in the rate of TS, between 10.5% and commonly defined as the occurrence of an intraocular 46%, can be found in the literature. This can be attributed to hemorrhage associated with a subarachnoid hemorrhage the fact that the definition of TS has shifted in clinical (SAH).1,2 Clinically, may be sub- practice from being solely a vitreous hemorrhage (VH) to retinal, intraretinal, preretinal, subhyaloid, or intravitreal, and, including any type of VH or retinal hemorrhage (vitreous, at present, any type of intracranial hemorrhage accompanied intraretinal, preretinal, subhyaloidal);3,4 VH is found in 3% by vitreous or retinal hemorrhage is known as TS.3,4 Ac- to 5% of cases.9e13 There is an association among intra- cording to the literature, TS also may be caused by intrace- ocular hemorrhage, the severity of intracranial hemorrhage, rebral hemorrhage, subdural or epidural hematoma, severe and the mortality rate. Patients with higher Hunt and Hess brain , or intraventricular hemorrhage.5 The mechanism grades exhibit a higher frequency of intraocular bleeding causing intraocular bleeding remains unclear, but the and mortality rate. prevailing hypothesis is that TS is the result of retinal Currently, there are no clear guidelines for the timing of venous caused by displaced blood that is ophthalmological interventions.9,14,15 Spontaneous clearance forced into the liquor spaces of the and causes of VH may be expected within 10 to 12 months, but vitreous

1628 2014 by the American Academy of Ophthalmology ISSN 0161-6420/14/$ - see front matter Published by Elsevier Inc. http://dx.doi.org/10.1016/j.ophtha.2014.02.015 Skevas et al Terson’s SyndromedRate after Subarachnoid Hemorrhage and Surgery surgery can expedite this process, especially in cases of Results nonclearing hemorrhage. This may prevent some of the se- vere complications, including forma- The rate of TS was 19.6% (20/102) with a predominance among tion, macular holes, proliferative vitreoretinopathy (PVR), female patients (16/66 female patients, 4/36 male patients; P ¼ 0.113). , hemosiderosis, optic atrophy, and devel- Themeanageofthepatientswas52.111.8 years (range, 23e87 10,11,16e18 years). Patients presenting initially with a GCS score of less than 8 opment of in younger patients. Prolif- ¼ df ¼ P ¼ eration of glial cells and elements of the retinal pigment (chi-square 13.328; 1; 0.001), a high Hunt and Hess grade (chi-square ¼ 23.622; df ¼ 1; P<0.001), and a high Fisher grade (chi- epithelium are capable of causing retinal distortion and square ¼ 9.389; df ¼ 1; P ¼ 0.002) were more often effected by TS. As fi 18 brotic adhesion. a consequence of the lower initial GCS score, the higher Hunt and The aim of our interdisciplinary study was to analyze the Hess grade, and higher Fisher grade, patients with TShad a statistically need for surgical intervention in TS, the effect of vitrectomy significantly worse Glasgow Outcome Scale score after 3 months (chi- with or without internal limiting membrane (ILM) peeling, square ¼ 12.706; df ¼ 1; P ¼ 0.001) (Table 1). the appearance of complications (intraoperative or post- operative), the rate of TS, the correlations between TS and sex, and the influence of severity of SAH expressed by Glasgow Coma Scale (GCS) score and Hunt and Hess grade Table 1. Characteristics of Patients with Subarachnoid Hemor- on the occurrence of TS. All of our patients were hospital- rhage (Aneurysmal and Perimesencephalic Subarachnoid ized for SAH. Hemorrhage) No. of Patients Methods Characteristic No TS With TS This uncontrolled interdisciplinary prospective study was approved Sex by the local ethics committee of the medical council of the state of Male 32 4 Hamburg (PV3611 and PV4079). All patients with SAH admitted 88.9% 11.1% to our hospital over a period of 24 months were screened for TS if Female 50 16 written consent was signed by the patient or legal representative. In 75.8% 24.2% GCS score at admission total, 102 patients were included in this study. Ophthalmological examination (OE) was performed on days 1 and 14, including best- 87311 86.9% 13.1% corrected visual acuity (BCVA); in patients sufficiently responsive <899 to following standardized OE, anterior chamber evaluation and 50.0% 50.0% fundoscopy (assessment of optic nerve head, macula, and peripheral Hunt and Hess grade ) were performed after medical (Mydriaticum I342 Stulln) and pupillary reaction. The examination on day 14 was 94.4% 5.6% performed to detect TS developing after a delay of several days, II 24 2 which has been described elsewhere. In cases of VH in which 92.3% 7.7% retinal examination was not possible, B-scan ultrasonography was III 13 5 performed. All patients with TS were asked to come back to the 72.2% 27.8% ophthalmology department for a follow-up visit after 3 months or as IV 10 4 soon as they were discharged from the rehabilitation centers. 71.4% 28.6% In cases of nonresorbing VH lasting at least 3 months (mean V17 interval between SAH and vitrectomy was 4.4 months; range, 3e5 12.5% 87.5% months), a standard 23-gauge 3-port pars plana vitrectomy (PPV) Fisher grade at admission was performed (9 eyes of 8 patients) using an Accurus system 160 (Alcon, Fort Worth, TX). If sub-ILM deposits of blood or puckering 100% 0% of the ILM was observed during surgery (after clearing the dense 2130 VH), an additional peeling of the ILM was performed (4 cases). The 100% 0% ILM was stained with the help of ILM-BLUE (DORC, Zuidland, The 3202 90.9% 9.1% Netherlands) and peeled with end-gripping ILM forceps. All patients 44018 underwent a complete OE preoperatively and postoperatively and 69.0% 31.0% optical coherence tomography (OCT) examination (Cirrus OCT; GOS after 3 mos Carl Zeiss Meditec, Dublin, CA) postoperatively to evaluate the 101 effect of the vitrectomy and the ILM peeling. 0% 100% 254 Statistics 55.6% 44.4% 395 Statistical analyses of the data were performed using a Student t e 64.3% 35.7% test, chi-square test, or trend tests (Mantel Haenszel chi-square), 4185 depending on the scale of the measurements, to examine correla- 78.3% 21.7% tions between the parameters using SPSS Statistics 21 (IBM, 5505 Chicago, IL). For statistics, visual acuity (VA) values were trans- 90.9% 9.1% formed to a logarithm of the minimum angle of resolution (log- MAR) scale and compared using a Student t test. The level of ¼ ¼ ¼ statistical significance was set at P<0.05. For figures, the VA GCS Glasgow Coma Scale; GOS Glasgow Outcome Scale; TS Terson’s syndrome. scores were used on a decimal scale for better visualization.

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Table 2. Ophthalmological Parameters in Patients with Terson’s Syndrome

Time to Preoperative Postoperative ILM Patient Sex Eye Vitrectomy VA VA Peeling Follow-up Comments 1 Female Right 4 2.2 0.0 No 7 Phacoemulsification of IOL after PPV 2 Male Right 4 2.4 0.0 No 8 Phacoemulsification with phacoemulsification of IOL 3 Male Right 5 2.2 0.1 No 3 4 a Female left 5 2.2 0.1 Yes 12 Phacoemulsification of IOL after PPV 4 b Female Right 4 2.0 0.1 No 12 Phacoemulsification of IOL after PPV 5 Male Left 4 0.3 0.1 Yes 5 6 Female Right 3 2.2 0.0 Yes 4 7 Female Right 5 2.2 0.2 Yes 12 8 Female Right 4 2.2 0.1 No 6

ILM ¼ internal limiting membrane; IOL ¼ intraocular ; PPV ¼ pars plana vitrectomy; VA ¼ visual acuity.

The first OE was performed on the day that written consent was Visual acuity improved in all patients. The BCVAs at first obtained, a mean of 7.26 days after SAH (standard error of the presentation and last presentation were 2.2 and 0.0625 logMAR, mean 37.28). In 57 patients (55.9%), OE was repeated 14 days respectively. The BCVAs at the first and last presentations of the after the first OE (15.5610.46 days). The second examination was patients undergoing ILM peeling were 1.725 and 0.05 logMAR, performed in every patient who was still admitted to our hospital. respectively (all patients [n = 9], P<0.001; with ILM peeling Because of ethic committee regulations, no changes to the usual [n ¼ 4], P ¼ 0.029; without ILM peeling [n ¼ 5], P<0.001) clinical course were allowed. The third OE was planned to be (Table 2). performed 3 months after the onset of the SAH. A total of 15 of the 20 patients (75%) with TS returned for OE after 3 months or as soon as possible after discharge from the rehabilitation unit Discussion (135.5356.85 days after SAH). Patients with SAH without TS had no ocular pathologies or monocular . Several patients had binocular The prevalence of TS, defined as any kind of intraocular double vision due to motoric nerve palsy. hemorrhage, is between 10.5% and 46%, and VH may be e Of the 20 patients with TS, 8 (9 eyes; 40% of the patients with associated with 3% to 5% of the cases.9 13 Our study TS) underwent a standard 3-port, 23-gauge PPV because of non- showed a rate of TS of 19.6% (20/102) and a higher rate of clearing vitreous bleeding. In 4 patients (4 eyes; 20% of patients VH in these patients with TS (40%). Prevalence often may with TS), ILM peeling was necessary because of sub-ILM bleeding be underestimated because of the severity of the underlying or puckering of the ILM. The mean interval between SAH and e condition, and if neurosurgical centers do not perform an vitrectomy was 4.4 months (range, 3 5 months). All procedures OE routinely, only a minority of patients will be diagnosed were performed by a single surgeon (L.W.). The type of anesthesia 14,19 was chosen in consultation with patients, but general anesthesia was at the time of SAH. The presence of vitreous bleeding is a sign of the severity of the disease, as clearly demonstrated used only if there were no neurologic or other systemic safety 1 concerns. Seven operations were performed under general anes- by our results. According to Frizzell et al, the higher rate thesia, and 2 operations were performed with retrobulbar block. of VH in our study may be related to improved survival The mean time for PPV was 33.95.6 minutes (range, 20e60 rates of the patients and may be a sign of improved minutes). None of the patients were pseudophakic at the time of interdisciplinary treatment regimens. vitrectomy. One procedure was combined with intraocular lens The precise mechanism of TS remains obscure and has implantation, and 2 patients (3 eyes) who developed been under debate for many years. Manschot13 hypothesized received an intraocular lens implantation during the postoperative that a spontaneous subarachnoid bleeding causes sudden follow-up. Cryotherapy was performed in 4 patients (50%) because intracranial hypertension and that blood is forced under high of the intraoperative detection of retinal lesions (e.g., lattice de- pressure into the subarachnoid space of optic nerves. This generations, no retinal breaks) in the outmost periphery to reduce 20 the risk of postoperative retinal complications while putting the lens was challenged by Hedges and Walsh on the grounds that at as low a risk as possible. In the case requiring combined pressure is not transmitted down the sheath space because surgery and vitrectomy, a hexafluoroethane gas tamponade and there is no connection between the subarachnoid space and laser treatment had to be used because of a peripheral retinal intraocular structures and that VH occurs through a rapid detachment that was not noted during the preoperative echography increase of intracranial pressure transmitted throughout the but was seen as soon as the retina became visible during surgery. venous channels into the orbital veins. Michalewska et al,8 Optic nerve atrophy was not observed in any of the patients. No using spectral domain OCT, suggested that blood may enter intraoperative complications were observed, and except for the 3 the vitreous cavity around the retinal vessels near the optic cases of cataract surgery, no patients had to undergo a subsequent disc. Inside the eye, the blood may spread intraretinally, reoperation because of complications (e.g., PVR, retinal detach- ment, or epiretinal membranes). below the ILM, or along retinal vessels. Postoperatively, patients were followed up for 6.4 months Vitrectomy for visual rehabilitation after VH in patients (range, 3e12 months). The postoperative OCT scans showed no with TS accelerates visual recovery, but there is still con- 10,15 signs of epiretinal membranes, , or other signs of troversy as to the optimal timing for surgical interven- pathology. tion. Several factors need to be considered. Early vitrectomy

1630 Skevas et al Terson’s SyndromedRate after Subarachnoid Hemorrhage and Surgery

can lead to substantial rehabilitation of VA and reduces the risks for complications that can occur if surgery is delayed (e.g., PVR, retinal detachment, ghost cell , and epiretinal membrane formation). However, some authors suggest performing a vitrectomy only after failure of spon- taneous resorption of hemorrhage.17,21e24 The time course for spontaneous resorption is variable and may take years to complete,11,21 although clearance rates of 10 to 12 months have been reported.11,16 Current recommenda- tions suggest 3 to 6 months of observation after the acute event. Vitrectomy should follow if there is no resorption of hemor- rhage or improvement of VA by this time.24,25 The vitrectomy technique has evolved enormously over the last few decades (higher cutting rates, shorter operation time, less trauma because of smaller gauge trocars, and lower complication rates). This fact could also argue for earlier intervention. Augsten et al,26 describing 6 eyes from 3 patients, concluded that for patients with bilateral TS without spontaneous resorption, surgery should be performed in at least 1 eye no later than 4 to 8 weeks after SAH. Daus et al27 suggested delaying vitrectomy in patients with unilateral hemorrhage and early vitrectomy in patients with bilateral vitrectomy. The time span in our study between SAH occurrence (diagnosis of TS) and surgical intervention was 4.4 months. This interval was used because rehabilitating measures for all of our patients were planned to take place after discharge from the hospital, and sometimes patients were in a poor general state of health. If the ensuing OE showed no signs of resorption, surgical intervention was scheduled. Our data show that all of our patients benefited from surgery, with a significant increase in BVCA (preoperative 2.2 and postoperative BCVA 0.0625 logMAR) (Fig 1A). We observed no intraoperative complications. Well-known complications of TS, such as epiretinal membrane formation, PVR, and retinal detachment, are the result of the proliferation of glial cells and elements of the retinal pigment epithelium causing retinal distortion and fibrotic adhesions.18 There are also reports of sub-ILM and subhyaloid hemorrhages. Friedman and Margo28 reported a dissection between the ILM and the underlying Müller cell end plates, and Srinivasan and Kyle29 reported both a sub- ILM and subhyaloid hemorrhage in patients with TS. Yokoi et al30 suggested that as a consequence of the VH and the breakdown of the ILM, glial cell migration and proliferation into the vitreous cavity result in epiretinal membrane formation and PVR. In a case report using immunohistochemistry, Arroyo and Bula31 analyzed a pigmented macular membrane overlying intraretinal blood after performing vitrectomy and membrane peeling. The histologic and immunohistochemical analyses revealed a membrane consistent with the ILM. Another finding of this study was that the dissection plane in TS was between the ILM and the Müller cell end plates.

Figure 1. Comparison of visual acuity (VA) (decimal scale) before and after vitrectomy for dense vitreous hemorrhage (VH) in patients with Terson’s syndrome (TS). A, All patients. B, Patients who underwent operation without internal limiting membrane (ILM) peeling. C, Patients who had an additional ILM peeling.

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In cases of vitreous bleeding with or without sub-ILM 2. Ko F, Knox DL. The ocular pathology of Terson’s syndrome. bleeding, vitrectomy with or without membrane peeling Ophthalmology 2010;117:1423–9. and peeling of the ILM needs to be performed to remove the 3. Weingeist TA, Goldman EJ, Folk JC, et al. Terson’s syn- drome. Clinicopathologic correlations. Ophthalmology VH, the epiretinal gliosis, and the sub-ILM bleeding. The – combination of new microsurgical instrumentation and 1986;93:1435 42. 4. Keithahn MA, Bennett SR, Cameron D, Mieler WF. Retinal different dyes facilitates the peeling and increases the per- – 32 33 folds in Terson syndrome. Ophthalmology 1993;100:1187 90. formance and end results of surgery. Garweg and Koerner 5. Kim HS, Lee SW, Sung SK, Seo EK. Terson syndrome caused analyzed the data for 37 patients (45 eyes) with TS and VH in by intraventricular hemorrhage associated with moyamoya a retrospective 30-year study and concluded that 85% of the disease. J Korean Neurosurg Soc 2012;51:367–9. patients experienced a rapid and persisting visual recovery. 6. Muller PJ, Deck JH. Intraocular and optic nerve sheath hem- The 4 patients in our study who underwent ILM peeling orrhage in cases of sudden intracranial hypertension. for sub-ILM bleeding showed an increase in BCVA J Neurosurg 1974;41:160–6. from 1.725 to 0.05 logMAR (Fig 1C). Postoperatively and 7. Ogawa T, Kitaoka T, Dake Y, Amemiya T. Terson syndrome: a case report suggesting the mechanism of vitreous hemor- during the follow-up period, 3 patients underwent cataract – surgery because of the development of lens opacification after rhage. Ophthalmology 2001;108:1654 6. 8. Michalewska Z, Michalewski J, Nawrocki J. Possible methods vitrectomy. There were no complications after cataract of blood entrance in Terson syndrome. Ophthalmic Surg La- surgery. sers Imaging 2010;41(Suppl):S42–9. For premacular subhyaloid hemorrhages, spontaneous 9. Roux FX, Panthier JN, Tanghe YM, et al. Terson’s syndrome resorption may be slow and may result in long-standing and intraocular complications in meningeal hemorrhages visual impairment. Ulbig et al34 concluded that puncturing (26 cases) [in French]. Neurochirurgie 1991;37:106–10. the posterior hyaloid face or the ILM using a pulsed 10. Kuhn F, Morris R, Witherspoon CD, Mester V. Terson syn- neodymium-doped yttrium aluminum garnet laser is a drome: results of vitrectomy and the significance of vitreous viable alternative treatment to vitrectomy, provided that the hemorrhage in patients with subarachnoid hemorrhage. – bleeding is not dense enough to block the laser beam. Ophthalmology 1998;105:472 7. The care of patients after SAH requires an intensive 11. Schultz PN, Sobol WM, Weingeist TA. Long-term visual outcome in Terson syndrome. Ophthalmology 1991;98:1814–9. coordination of effort among specialties, from neurosur- 12. Fahmy JA. Fundal haemorrhages in ruptured intracranial an- geons, neurologists, radiologists, and ophthalmologists to eurysms. II. Correlation with the clinical course. Acta Oph- rehabilitating centers. Our 24-month prospective study thalmol (Copenh) 1973;51:299–304. contributes to the complex management of TS with, to our 13. Manschot WA. Subarachnoid hemorrhage; intraocular symp- knowledge, one of the highest numbers of recruited patients toms and their pathogenesis. Am J Ophthalmol 1954;38:501–5. and a close interdisciplinary collaboration of ophthalmolo- 14. Wietholter S, Steube D, Stotz HP. Terson syndrome: a gists and neurosurgeons. frequently missed ophthalmologic complication in subarachnoid hemorrhage [in German]. Zentralbl Neurochir 1998;59:166–70. 15. Sharma T, Gopal L, Biswas J, et al. Results of vitrectomy in Study Limitations Terson syndrome. Ophthalmic Surg Lasers 2002;33:195–9. 16. Khan SG, Frenkel M. Intravitreal hemorrhage associated with One of the limitations of our study is that it is an uncon- rapid increase in intracranial pressure (Terson’s syndrome). trolled study. Also, the number of patients, although being Am J Ophthalmol 1975;80:37–43. one of the most extensive prospective studies of the rate of 17. Ritland JS, Syrdalen P, Eide N, et al. Outcome of vitrectomy in TS and outcome of vitrectomy in TS, is still not high. patients with Terson syndrome. Acta Ophthalmol Scand Therefore, any conclusions based on the data presented must 2002;80:172–5. be drawn with caution. 18. Rubowitz A, Desai U. Nontraumatic macular holes associated In conclusion, this prospective uncontrolled study shows with Terson syndrome. Retina 2006;26:230–2. that vitrectomy, and ILM peeling if needed, had advanta- 19. Nowosielska A, Czarnecki W. Terson syndrome [in Polish]. – geous effects on the visual rehabilitation of all patients with Klin Oczna 2003;105:79 81. nonclearing VH after TS. The rate of TS (19.6%) is com- 20. Hedges TR Jr, Walsh FB. Optic nerve sheath and subhyaloid hemorrhage as a complication of angiocardiography. AMA parable to that in other reports, but the rate of VH is high Arch Ophthalmol 1955;54:425–7. (40%). So far, no consensus among vitreoretinal surgeons as 21. Nacef L, Zghal-Mokni I, Allagui I, et al. Indications and re- to the optimal timing for surgical intervention exists, but in sults of vitrectomy in Terson syndrome [in French]. Tunis Med our cases of dense nonclearing hemorrhage that persists for 2004;82:461–4. more than 3 months, we did not identify any safety concerns 22. Velikay M, Datlinger P, Stolba U, et al. Retinal detachment after PPV. with severe proliferative vitreoretinopathy in Terson syn- drome. Ophthalmology 1994;101:35–7. 23. Murjaneh S, Hale JE, Mishra S, et al. Terson’s syndrome: References surgical outcome in relation to entry site pathology [letter]. Br J Ophthalmol 2006;90:512–3. 24. Augsten R, Konigsdorffer E. Terson syndromeea contribution 1. Frizzell RT, Kuhn F, Morris R, et al. Screening for ocular to the timing of operation for pars plana vitrectomy [in hemorrhages in patients with ruptured cerebral : a German]. Klin Monbl Augenheilkd 2007;224:674–7. prospective study of 99 patients. Neurosurgery 1997;41: 25. Fountas KN, Kapsalaki EZ, Lee GP, et al. Terson hemorrhage 529–34. in patients suffering aneurysmal subarachnoid hemorrhage:

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predisposing factors and prognostic significance. J Neurosurg 30. Yokoi M, Kase M, Hyodo T, et al. Epiretinal membrane for- 2008;109:439–44. mation in Terson syndrome. Jpn J Ophthalmol 1997;41: 26. Augsten R, Konigsdorffer E, Strobel J. Surgical approach in 168–73. Terson syndrome: vitreous and retinal findings. Eur J Oph- 31. Arroyo JG, Bula DV. Immunohistochemical study of the in- thalmol 2000;10:293–6. ternal limiting membrane in Terson syndrome. Retina 2004; 27. Daus W, Kasmann B, Alexandridis E. Terson syndrome. 24:155–7. Complicated clinical course [in German]. Ophthalmologe 32. Abdelkader E, Lois N. Internal limiting membrane peeling in 1992;89:77–81. vitreo-retinal surgery. Surv Ophthalmol 2008;53:368–96. 28. Friedman SM, Margo CE. Bilateral subinternal limiting 33. Garweg JG, Koerner F. Outcome indicators for vitrectomy in membrane hemorrhage with Terson syndrome. Am J Oph- Terson syndrome. Acta Ophthalmol 2009;87:222–6. thalmol 1997;124:850–1. 34. Ulbig MW, Mangouritsas G, Rothbacher HH, et al. Long-term 29. Srinivasan S, Kyle G. Subinternal limiting membrane and results after drainage of premacular subhyaloid hemorrhage subhyaloid haemorrhage in Terson syndrome: the macular into the vitreous with a pulsed Nd:YAG laser. Arch Oph- ‘double ring’ sign. Eye (Lond) 2006;20:1099–101. thalmol 1998;116:1465–9.

Footnotes and Financial Disclosures

Originally received: September 18, 2013. Abbreviations and Acronyms: Final revision: February 14, 2014. BCVA ¼ best-corrected visual acuity; GCS ¼ Glasgow Coma Scale; Accepted: February 14, 2014. ILM ¼ internal limiting membrane; logMAR ¼ logarithm of the minimum Available online: April 1, 2014. Manuscript no. 2013-1596. angle of resolution; OCT ¼ optical coherence tomography; 1 University Medical-Centre Hamburg-Eppendorf, Department of Ophthal- OE ¼ ophthalmological examination; PPV ¼ pars plana vitrectomy; mology, Hamburg, Germany. PVR ¼ proliferative vitreoretinopathy; SAH ¼ subarachnoid hemorrhage; 2 TS ¼ ’ VA ¼ VH ¼ University Medical-Centre Hamburg-Eppendorf, Department of Neuro- Terson s syndrome; visual acuity; vitreous hemorrhage. surgery, Hamburg, Germany. Correspondence: *C.S. and P.C. contributed equally to this article. Christos Skevas, MD, University Medical-Centre Hamburg-Eppendorf, Financial Disclosure(s): Department of Ophthalmology, Martinistr. 52, D-20246 Hamburg, Ger- The author(s) have no proprietary or commercial interest in any materials many. E-mail: [email protected]. discussed in this article.

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