Role of Imaging in Identifying Blood Flow Direction In Terson’s Syndrome

A case series demonstrates disease-specific use of imaging.

ZOFIA MICHALEWSKA, MD, PhD · JANUSZ MICHALEWSKI, MD · JERZY NAWROCKI, MD, PhD

In 1881, Moritz Litten first suspected an association between the vitreous and subarachnoid hemorrhage.¹ Nineteen years later, Albert Terson, a French ophthalmologist, provided a more precise description of the association.²

Terson’s syndrome is an intraocular hemorrhage arising secondary to intracranial hemorrhage, which may occur either during severe trauma or during the course of cerebral aneurysms. The disease is mostly bilateral.

Terson’s syndrome occurs in approximately 3% to 20% patients with acute intracranial bleeding.^3-5 Given the high mortality rate in this patient population, those numbers may be underestimated.

WHERE DOES THE BLOOD COME FROM?

Some authors have postulated that intraocular hemorrhage emanates from the direct dissection of subarachnoid hemorrhage down the optic nerve sheath. In this model, the amount of fluid in the subarachnoid space of the optic nerves leads to closure of the central retinal vein, and rising blood pressure results in rupture of this vein and vitreous hemorrhages.^6,7

Elevation of intracranial pressure correlates directly with the severity of intraocular bleeding.⁸ The existence of open communication from the subarachnoid space into the optic canal has been proved. Manschot injected a mixture of ink and gelatin into the subarachnoid space of a cadaver and observed ink in the optic canal.⁶

HOW DOES BLOOD SPREAD INSIDE THE EYE?

In patients with Terson Syndrome, exact visualization of the ways in which blood spreads inside the eye is impossible prior to vitrectomy, due to opaque media. Precise examinations may be performed during or for the first few days after surgery.

A few years ago, our group was the first to present spectral-domain OCT and scanning laser ophthalmoscopy findings of several patients with Terson’s syndrome.⁹ A video based on this paper was presented with the Rhett Buckler Award at the ASRS meeting in 2010.

Blood May Spread Directly Though Optic Disc

During surgery, we have noted blood infiltrates the vitreous body and adheres strongly to the optic disc in all cases. Some SD-OCT scans have presented hyper-reflective detached fragments of tissue over the optic nerve head (Figure 1, page 40).

Figure 1. Intraoperative image and SD-OCT of a 29-year-old man after a traffic accident. Top: A small blood clot is probably present over the optic disc nerve in this intraoperative image. Bottom: the yellow arrow indicates the same structure visible during surgery and postoperatively on SD-OCT.

This is quite an unusual finding, because we have not observed these fragments when performing OCT after vitrectomy for other indications – for example, macular hole or epiretinal membrane.

Without histopathology, we can only speculate as to the origin of the hyper-reflective fragments over the optic disc. These fragments are either small fragments of residual vitreous or blood clots. However, we successfully performed posterior hyaloid detachment in all cases.

The only disease in which we have observed a similar hyper-reflective tissue over the optic disc nerve after vitrectomy is optic pit–associated maculopathy (Figure 2). It is suspected that subarachnoid fluid enters the eye in patients with optic pit associated–maculopathy and that in Terson’s syndrome, blood spreads into the eye from the intracranial space. Thus, similar SD-OCT images of the optic nerve are not surprising.

Figure 2. OCT of the eye of a 33-year-old woman one week after surgery for maculopathy associated with optic pit.

In optic pit–associated maculopathy, this structure has been described as the “inner limiting membrane of Elschnig.” The membrane is a continuation of internal limiting membrane over the optic disc.¹⁰

Blood May Spread Along Retinal Vessels

The spread of blood, not directly from the optic nerve but from vascular arcades away from the optic disc, was an intrasurgical observation first made by Ferenc Kuhn.⁴

We confirmed this observation intrasurgically and documented it with HRT images that show hyporeflective spots corresponding to blood spots observed during surgery (Figure 3, page 42). The Heidelberg Retina Tomograph (HRT 2, Heidelberg Engineering, Heidelberg, Germany) scanning laser microscope additionally presents topographic images of the surface of the optic nerve and fovea.

Figure 3. Intrasurgical image presenting blood spots along retinal vessels (yellow arrows). HRT image (right) of the same patient one week after surgery. Yellow arrows indicate hyporeflective spots around the fovea.

Blood May Spread Under the ILM

The results of intentionally performed ILM peeling in Terson’s syndrome have been reported as satisfactory.⁴ ILM peeling should be considered especially in patients in whom blood has spread underneath the ILM.

During surgery, blood may no longer be visible, but detached ILM may be observed intrasurgically and on postoperative SD-OCT. Previous histopathological findings have also found blood accumulated between the ILM and Müller cells.¹¹ The blood may have entered directly through the optic nerve but first entered the area under the ILM, detached it, and then spread into the vitreous.

In our group of patients, those in whom blood had spread under the ILM had a persistent slightly elevated foveal contour after surgery (Figure 4). Its appearance was quite similar to that observed after idiopathic epiretinal membrane removal. All of the patients in whom blood did not accumulate below the ILM had a normal foveal contour.

Figure 4. Postoperative fovea contour on SD-OCT, from a patient in whom blood had accumulated under the ILM. The slightly elevated foveal contour is visible (top). Normal postoperative foveal contour on SDOCT from a patient with Terson’s syndrome (bottom).

Blood May Spread Subretinally

Additionally, intrasurgical observations in our patients revealed that blood also spreads subretinally. In one patient, during Trypan blue-assisted removal of ERM, we observed that this was not only localized at the retinal surface but also subretinally.

In summary, we have presented four possible ways in which blood may enter into the eye in Terson’s syndrome:
•   directly though the optic disc;
•   along the blood vessels; under the ILM; and
•   subretinally.

The last route has not been described previously.

The use of SD-OCT and SLO enables visualization of the postoperative status of eyes with Terson’s syndrome.

FINAL RESULTS

Our group consisted of 11 eyes of six patients with Terson’s syndrome. The patients’ final visual outcomes were satisfactory in all cases (0.8-1.0 Snellen VA).

Spectral-domain OCT revealed small photoreceptor and ELM defects in two eyes. However, in the presented cases, these defects were too small to influence the visual outcomes.

The origin of the defects is unclear. However, we speculate that the toxic effects of subretinal blood could have induced the defects. Foveal contour and the structure of the particular layers were normal in all eyes, even those in which blood had accumulated below the ILM. In these cases, the foveal contour remained slightly irregular and elevated after surgery, although this change did not influence final visual acuity. RP

REFERENCES

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2. Terson A. De l’hémorrhagie dans le corps vitre au cours de l’hémorrhagie cerebrale. Clin Ophthalmol 1900;6:309-312.

3. Regillo CD. Distant trauma with posterior segment effects. In: Yanoff M, Duker JS, eds. Ophthalmology. Philadelphia, PA; Mosby; 1999;8:1-6.

4. Kuhn F, Morris R, Witherspoon CD, et al. Terson syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. Ophthalmology. 1998;105:472-477.

5. Fahmy JA. Fundal haemorrhages in ruptured intracranial aneurysms I. Material, frequency, and morphology. Acta Ophthalmol. 1973;51:289-98.

6. Manschot WA. Subarachnoid hemorrhage. Intraocular symptoms and their pathogenesis. Am J Ophthalmol. 1954;38:501-505.

7. Espinasse-Berrod MA, David T, Parent de Curzon H, et al. Terson’s syndrome. Apropos of 7 cases. J Fr Ophthalmol. 1980;11:43-51.

8. Ogawa T, Kitaoka T, Dake Y, et al. Terson syndrome: A case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology. 2001;108:1654-1656.

9. Michalewska Z, Michalewski J, Nawrocki J. Possible methods of blood entrance in Terson syndrome. Ophthalmic Surg Lasers Imaging. 2010;41(Suppl):S42-S9.

10. Ferry AP. Macular detachment associated with congenital pit of the optic nerve head. Arch Ophthalmol. 1963;70:106-117.

11. Arroyo JG, Bula DV. Immunohistochemical study of the internal limiting membrane in Terson syndrome. Retina. 2004;24:155-157.