J Neurosurg 88:851Ð854, 1998, Click here to return to Table of Contents

Terson’s syndrome in subarachnoid hemorrhage and severe brain injury accompanied by acutely raised intracranial pressure

RALPH J. MEDELE, M.D., WALTER STUMMER, M.D., ARTHUR J. MUELLER, M.D., HANS-JAKOB STEIGER, M.D., AND HANS-JÜRGEN REULEN, M.D. Department of Neurosurgery, Klinikum Grosshadern, Ludwig-Maximilians University Munich, Munich, Germany

Object. The syndrome of retinal or vitreous hemorrhage in association with subarachnoid hemorrhage (SAH) is known as Terson’s syndrome. The authors’ purpose was to determine whether occurs with similar incidence when caused by severe brain injury accompanied by acutely raised intracranial pressure (ICP). Methods. Prospective ophthalmological examination was performed in 22 consecutive patients with SAH or severe brain injury and elevated ICP. Thirteen patients were admitted for SAH (World Federation of Neurological Surgeons Grades IIÐIV) and nine for severe brain injury (Glasgow Coma Scale scores 3Ð10). Monitoring of ICP was performed at the time of admission via a ventricular catheter. Initial ICP exceeded 20 mm Hg in all patients. Indirect ophthalmoscopy without induced was performed within the 1st week after the acute event. Retinal or vitreous hemorrhage was seen in six (46%) of 13 patients with SAH and in four (44%) of nine patients with severe brain injury. Ocular bleeding was found bilaterally in three patients with SAH and in one patient with severe brain injury (18%). Six of the 10 patients with Terson’s syndrome died as a result of their acute event. Conclusions. The present results indicate that Terson’s syndrome may be related to acute elevation of ICP, inde- pendent of its causes, and may occur with similar incidence in patients with severe brain injury and those with SAH. Because recognition and treatment of Terson’s syndrome may prevent visual impairment and associated secondary damage to the eye, increased awareness of this entity in all patients with acute raised intracranial hypertension is recommended.

KEY WORDS ¥ Terson’s syndrome ¥ subarachnoid hemorrhage ¥ severe brain injury ¥ intracranial pressure

N 1881 the German ophthalmologist, Moritz Litten,22 or severe brain injury, were admitted to our institution and first described vitreous bleeding occurring with sub- entered into the study in 1994. Acute intracranial hyper- I arachnoid hemorrhage (SAH). The observation of vit- tension was defined as ICP initially exceeding 20 mm Hg, reous hemorrhage in conjunction with any form of in- as observed during ventricle catheter implantation or dur- tracranial bleeding was named after Albert Terson.35 The ing the first ICP measurements in the intensive care unit definition has been expanded by some authors to include (ICU). Thirteen patients with SAH were assigned Grades intraretinal hemorrhage.5 II to IV according to the scale of the World Federation of Espinasse-Berrod and associates10 suggested that rapid Neurological Surgeons9 and 2 to 4 according to Fisher increases in intracranial pressure (ICP) cause decreased grading on CT scanning.11 The nine patients with severe venous drainage of the eyes’ posterior compartments be- brain injury had initial Glasgow Coma Scale34 scores of 3 cause of venous congestion. This may result in vitreous to 10. Intracranial diagnosis and staging were established hypertension and retinal or vitreous hemorrhage. by the injuries’ appearance on CT scanning. All patients The purpose of the present study was to elucidate with impaired consciousness and/or in whom hydroceph- whether this hypothesis can be supported by ICP mea- alus was identified on CT scanning underwent ICP moni- surement and whether Terson’s syndrome occurs with toring (intraventricular catheter system; Hanni Set, pvb similar frequency when caused by severe brain injury ac- Medizintechnik, Kirchseeon, Germany). The course of the companied by acutely raised ICP. ICP was recorded under steady conditions in the ICU for at least 3 days. All patients entered into the study were ex- Clinical Material and Methods amined by indirect ophthalmoscopy without induced my- driasis17,27 within the 1st week after the acute event. Visual Patient Population acuity and other function tests could not be performed Twenty-two patients, aged 29 to 80 years, suffering because most patients were in a coma. Ophthalmological from intracranial hypertension as a consequence of SAH follow-up examinations at 3 months could be performed

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FIG. 1. Ophthalmoscopic photograph obtained in a patient with severe head injury showing vitreous and retinal hemorrhage. in two surviving patients with Terson’s syndrome; the injury (mean maximum ICP 26.5 Ϯ 23.9 mm Hg; mean other two surviving patients were lost to follow up. initial ICP 19 Ϯ 16.6 mm Hg; and mean average ICP 14 Ϯ 11.4 mm Hg). Statistical Analysis Terson’s syndrome (Fig. 1) was observed in 10 (45%) All values are given as means Ϯ standard deviation. of 22 patients. Six (46%) of 13 patients with SAH and Statistical analysis was performed using the Whitney- four (44%) of nine patients with severe brain injury (44%) Mann-Wilcoxon test. A significant difference was as- had retinal or vitreous hemorrhage. Ocular bleeding was sumed with an error probability of less than 0.05. found bilaterally in three cases of SAH and in one case of severe brain injury (18%). There was no correlation be- tween the severity of the intracerebral pathological condi- Results tions graded on CT scans and the amount of intraocular There was no significant difference in maximum, ini- hemorrhage. tial, and average ICP within the first 72 hours in patients With one exception, initial coma was observed in all with SAH (mean maximum ICP 27 Ϯ 9.6 mm Hg; mean patients with intraocular hemorrhage. Seven patients with initial ICP 17 Ϯ 8.3 mm Hg; and mean average ICP 14 Ϯ ocular findings showed extremely raised ICP (Ͼ 30 mm 9.4 mm Hg) compared with patients with severe brain Hg) during ventricle catheter placement. The initial ICP

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Terson’s syndrome values measured in the ICU and the maximum measured ICP values were significantly higher in patients with Ter- son’s syndrome (mean initial ICP 26 Ϯ 6.9 mm Hg in patients with intraocular hemorrhage compared with 15 Ϯ 5.8 mm Hg in others; mean maximum ICP 32 Ϯ 15.5 mm Hg in patients with intraocular hemorrhage compared with 28 Ϯ 11.5 mm Hg in others; mean average ICP 16.5 Ϯ 11.3 mm Hg in patients with intraocular hemorrhage compared with 13 Ϯ 7.3 mm Hg in others; Fig. 2). The outcome of patients with intraocular bleeding was poor. Six of 10 patients died within the 3-month follow-up period. One surviving patient with SAH still had not re- gained vision in one eye at that time because of severe nonclearing vitreous hemorrhage. This patient later under- went pars plana and vision improved to 0.8 within the following weeks. The patient with brain injury FIG. 2. Graph demonstrating levels of ICP in patients with who was available for follow-up review showed no visual Terson’s syndrome compared with levels in patients without deterioration. Terson’s syndrome. Initial ICP in patients with Terson’s syndrome was significantly higher than in patients without Terson’s syn- drome. Discussion The occurrence of bleeding in posterior eye compart- ments is a known complication in patients surviving SAH. optic nerve sheath subarachnoid space and the vitreous The reported frequency of Terson’s syndrome in such pa- body.2,3 Castren5 suggested that rapid increases in ICP tients ranges between 20% and 50%,25,26,30,33 which is in result in Terson’s syndrome, which is caused by venous accordance with our results. However, this phenomenon congestion due to impairment of venous drainage to the has only rarely been described in association with subdu- cavernous sinus.10,12,16 Retinochoroidal connections and ral and epidural hematomas or traumatic SAH.10,21,32,36,38 the central retinal vein could be compressed by pressure- Only case reports are found in the literature. Billotte, et induced dilation of the optic nerveÐsheath subarachnoid al.,4 described Terson’s syndrome in an infant with severe space.24,36 Increased venous pressure results in stasis fol- brain injury. Another patient was reported to have intra- lowed by vessel rupture and intraocular hemorrhage. Our cerebral hemorrhage caused by coagulopathy as a conse- own observations support the concept that ICP represents quence of acute promyelocytic leukemia after retinoic the principal impetus for the development of intraocular acid treatment.1 Our results suggest that intraocular hem- hemorrhage because intraocular hemorrhage was associat- orrhage occurs with similar incidence when caused by ed with higher initial levels of ICP. However, our mea- severe brain injury compared with SAH and may be re- surements can only be taken as an indicator of the actual sponsible for vision impairment in such patients. intracranial pressure present when intraocular hemorrhage Coincident injury to the optic nerve and optic pathways developed. can be found in many cases of severe brain injury.2,20 Thus, In the initial phase of SAH, dramatic increases in ICP we cannot rule out that intraocular hemorrhage in these are noted for several minutes.14,15 Such a pressure pattern patients may have been a condition merely associated can also be observed in severe brain injury initially caused with more profound damage to the optic system. Unfor- by hypercarbia in the unconscious patient.23 Furthermore, tunately, afferent pupillary testing, which might have pro- posttraumatic Terson’s syndrome may result from plateau vided the respective information, was not performed in waves, which are well described in the early posttraumat- our study. On the other hand, the available literature on ic phase. Other patterns of intracranial hypertension with- Terson’s syndrome does not provide evidence for injury to out extreme ICP peaks, which are observed, for instance, afferent pathways in cases of severe SAH. Although liter- in hydrocephalus, cavernous sinus thrombosis, or carotid ature on the topic is sparse, Karel and Gergelyova18 report- cavernous sinus fistula, do not result in Terson’s syn- ed on seven patients with SAH and Terson’s syndrome. drome. A typical ophthalmological finding in such pa- All underwent pars plana vitrectomy. In six of their pa- tients is papilledema but not intraocular hemorrhage. tients, vision recovered to values between 0.7 and 1. In the The outcome of patients with Terson’s syndrome has only patient with severe brain injury who was available been reported to be poor. In many series the overall mor- for follow-up review in our study, no impairment of vision tality rate is significantly higher than that for patients was noted. In another patient with SAH, vision was only without Terson’s syndrome. Garfinkle and colleagues13 restored after pars plana vitrectomy had been performed. reported a 36.3% mortality rate in patients with intraocu- Initial attempts at explaining Terson’s syndrome sug- lar hemorrhage; Pfausler, et al.,28 reported death in nine of gested that, in SAH, blood traverses the subarachnoid 10 patients. In our study we observed a mortality rate of space into its continuation within the optic nerve sheath. It 60%. was thought that blood penetrates the sclera in the porous The prognosis for vision recovery in surviving patients region where the optic nerve enters the globe, and finally with SAH has been reported to be good.32,36 Most vitreous appears in the vitreous space within the eye.8 Many text- body bleedings clear spontanously within months. Con- books still attribute Terson’s syndrome to this mechanism, versely, the diagnosis of Terson’s syndrome may be im- despite evidence that there is no connection between the portant with regard to management because severe non-

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R. J. Medele, et al. clearing vitreous hemorrhage may result in blindness.7,13,25 17. Jacob J, Stead J, Sykes J, et al: A report on the use of technician In cases in which there is no tendency for blood resorp- ophthalmoscopy combined with the use of the Canon non- tion, the method of choice is a pars plana vitrectomy.18 mydriatic camera in screening for diabetic in the Most authors recommend a period of 6 months after the community. Diabet Med 12:419Ð425, 1995 19 18. Karel I, Gergelyova K: [Pars plana vitrectomy in Terson’s syn- acute event for the timing of surgery. If vitrectomy is drome.] Cesk Oftalmol 51:3Ð6, 1995 (Cze) performed, complete recovery of vision can be expected 6,19,26,31,37 19. Korner F, Meier-Gibbons F: [Vitrectomy in Terson syndrome. in many cases. Alternatively, intravitreous injec- Report of 18 cases.] Klin Monatsbl Augenheilkd 200: tions of anti-Rh serum have been reported to improve 468Ð471, 1992 (Ger) visual acuity within 5 to 6 weeks in cases of vitreous 20. Kowal L: Ophthalmic manifestations of head injury. Aust NZ J hemorrhage without proliferative vitreoretinopathy.29 Ophthalmol 20:35Ð40, 1992 Nevertheless, all patients should be closely monitored for 21. Le Rebeller MJ, Desplat A: [A case of post-traumatic Terson’s sequelae of intraocular bleeding. These include the devel- syndrome.] Bull Soc Ophthalmol Fr 80:1013Ð1015, 1980 (Fr) opment of intraocular hypertension and retinal membrane 22. Litten M: Ueber einige vom allgemein-klinischen Standpunkt formation with resulting .19,26 aus interessante Augenveränderungen. Berl Klin Wochenschr 18:23Ð27, 1881 With regard to our own observations, multiple intra- 23. Moskala M: [Minutes of the 2nd international symposium on cranial pathological conditions accompanied by acutely severe head injury in Parma, Italy, October 17-19, 1994.] Neu- raised ICP may result in intraocular hemorrhage. The fre- rol Neurochir Pol 29:283Ð284, 1995 (Pol) quencies were similar in patients who had severe brain 24. Muller PJ, Deck JHN: Intraocular and optic nerve sheath hem- injury compared with those who had SAH. For surviving orrhage in cases of sudden intracranial hypertension. J Neu- patients, close ophthalmological evaluation and treatment rosurg 41:160Ð166, 1974 are recommended. 25. Nogaki H, Tamaki N, Shirakuni T, et al: [Vitreous hemorrhage after ruptured intracerebral (Terson’s syndrome).] References No To Shinkei 33:223Ð227, 1981 (Jpn) 26. Oyakawa RT, Michels RG, Blase WP: Vitrectomy for nondia- 1. Abu El-Asrar AM, Al-Momen AK, Harakati MS: Terson’s syn- betic vitreous hemorrhage. Am J Ophthalmol 96:517Ð525, drome in a patient with acute promyelocytic leukemia on all- 1983 trans retinoic acid treatment. Doc Ophthalmol 84:373Ð378, 27. Parisi ML, Scheiman M, Coulter RS: Comparison of the effec- 1993 tiveness of a nondilated versus dilated fundus examination in 2. Anderson DP, Ford RM: Visual abnormalities after severe head the pediatric population. J Am Optom Assoc 67:266Ð272, injuries. Can J Surg 23:163Ð165, 1980 1996 3. Anderson DR: Ultrastructure of the optic nerve head. Arch 28. Pfausler B, Belcl R, Metzler R, et al: Terson’s syndrome in Ophthalmol 83:63Ð73, 1970 spontaneous subarachnoid hemorrhage: a prospective study in 4. Billotte C, Lecoq PJ, Sostenes C, et al: [Terson’s syndrome and 60 consecutive patients. J Neurosurg 85:392Ð394, 1996 a case of post-traumatic syndrome in an infant.] Bull Soc 29. Prost ME: [Clinical manifestations and treatment of Terson’s Ophthalmol Fr 88:111Ð114, 1988 (Fr) syndrome.] Klin Oczna 98:371Ð374, 1996 (Pol) 5. Castren JA: Pathogenesis and treatment of Terson-syndrome. 30. Roux FX, Panthier JN, Tanghe YM, et al: Complications intra- Acta Ophthalmol 41:430Ð434, 1963 oculaires dans les hémorrhagies méningées (26 cas). Neuro- 6. Cherestesi I, Pop M, Caltaru D: [Terson’s syndrome. Its surgi- chirurgie 37:106Ð108, 1991 cal resolution.] Ophthalmologia 38:318Ð321, 1994 (Rum) 31. 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Garfinkle AM, Danys IR, Nicolle DA, et al: Terson’s syn- 38. Vanderlinden RG, Chisholm LD: Vitreous hemorrhages and drome: a reversible cause of blindness following subarachnoid sudden increased intracranial pressure. J Neurosurg 41: hemorrhage. J Neurosurg 76:766Ð771, 1992 167Ð176, 1974 14. Grote E, Hassler W: The critical first minutes after subarach- noid hemorrhage. Neurosurgery 22:654Ð661, 1988 15. Hassler W, Steinmetz H, Gawlowski J: Transcranial Doppler Manuscript received April 17, 1997. ultrasonography in raised intracranial pressure and in intracra- Accepted in final form December 10, 1997. nial circulatory arrest. J Neurosurg 68:745Ð751, 1988 Address reprint requests to: Ralph J. Medele, M.D., Department 16. Hedges TR Jr: Mechanism of Terson’s syndrome. Ophthalmol of Neurosurgery, Klinikum Grosshadern, Ludwig-Maximilians 99:647, 1992 (Letter) University Munich, D-81377 Munich, Germany.

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