Ординатура / Офтальмология / Учебные материалы / Retinal Vascular Disease Joussen Springer

Core Messages

Purtscher’s retinopathy is a traumatic retinal angiopathy and was originally described in individuals with severe head trauma

Symptoms include rapid and painless vision loss

Usually occurs in both eyes, but unilateral cases have been reported

Acute funduscopic findings include cottonwool spots and intraretinal hemorrhages pri-

marily located in the posterior pole. Optic disk swelling may also occur

Purtscher’s-like retinopathy can occur in other traumatic conditions (compressive chest injuries, long bone fractures), collagen vascular diseases (systemic lupus erythematosus, sclerodermia, dermatomyositis), kidney diseases, and childbirth

Treatment is supportive and directed at the underlying medical condition

24.1.1 History

Purtscher’s retinopathy was first described by Otmar Purtscher in 1910 as a syndrome of multiple, white retinal patches, superficial retinal hemorrhages, and papillitis occurring in five patients with severe head trauma [11]. He originally named this condition angiopathia retinae traumatica and hypothesized that white, superficial retinal patches were lymphatic extravasations caused by a sudden increase in intracranial pressure secondary to massive head trauma.

The term Purtscher’s retinopathy or Purtscher’s- like retinopathy is currently used to describe similar fundus findings associated with various conditions: trauma (head trauma, compressive chest injuries, long bone fractures with fat embolism), collagen vascular diseases (systemic lupus erythematosus, sclerodermia, dermatomyositis), kidney disease, and childbirth (amniotic fluid embolism) [2, 4, 5, 8, 12].

Although associated with several systemic conditions, Purtscher’s retinopathy is a relatively uncommon finding and published reports in the literature have been limited to case reports.

24.1.2 Special Pathologic Features

Essentials

Complement-induced retinal leukoembolization is likely responsible for the ophthalmoscopic findings in Purtscher’s retinopathy

Although Otmar Purtscher initially postulated that the white, superficial retinal patches (now recognized as cotton-wool spots) were lymphatic extravasations caused by the sudden increase in intracranial pressure seen in severe head trauma [11], the exact pathogenesis of Purtscher’s retinopathy remains unknown. Several authors have hypothesized that microembolic events, such as fat embolization in long bone fractures and air embolization from compressive chest injuries, may be responsible [3]. Other scientists speculate that venous reflux with capillary engorgement of the upper body plays a role [10].

More recently, studies have shown that leukocyte aggregation by activated complement factor 5 (C5a) may lead to leukocyte emboli that can occlude the peripapillary retinal capillaries in conditions such as trauma, acute pancreatitis, and collagen vascular diseases [7]. Several authors have postulated that complement-induced retinal leukoembolization occurs in the setting of Purtscher’s retinopathy, and animal models have shown evidence of multiple small retinal arteriolar occlusions [6, 9].

Fig. 24.1.1. Fundus photograph demonstrating Purtscher’s retinopathy developing after an automobile accident. White, cot- ton-wool spots, intraretinal and preretinal hemorrhages, and arteriolar spasm are present primarily in the posterior pole

24.1.4 Differential Diagnosis

The differential diagnosis of Purtscher’s retinopathy includes retinal vascular disorders that can result in intraretinal hemorrhages and cotton-wool spots. Central retinal vein occlusion, hypertensive retinopathy, diabetic retinopathy, Valsalva retinopathy, and lupus retinopathy may all present with intraretinal hemorrhages and nerve fiber layer infarcts.

Differentiating between Purtscher’s retinopathy and other conditions requires a thorough medical history to document preexisting medical conditions, such as diabetes and hypertension, and possible precipitating events, such as trauma, that may suggest one disease over the other. In addition, funduscopic findings such as lipid exudates, tortuous and dilated veins, and retinal neovascularization are not typical-

ly seen in Purtscher’s retinopathy, and these findings may suggest diabetic retinopathy or venous occlusive disease instead. Ultimately, Purtscher’s retinopathy is a clinical diagnosis based on the medical history and examination findings.

Visual outcome in Purtscher’s retinopathy is variable depending on the location and amount of capillary non-perfusion, involvement of the macula, and degree of optic atrophy that can occur.

Currently there is no well-defined treatment for Purtscher’s retinopathy. Initial treatment is supportive and aimed at resolving the underlying medical condition.

Although several published studies have cited steroid therapy for the treatment of Purtscher’s retinopathy in hopes that steroids can stabilize damaged tissue and perhaps block the formation of comple- ment-activated leukocyte aggregation [1, 13], no large scale studies have been conducted to determine the efficacy of this type of treatment. Large clinical trials would be difficult to plan given the infrequent occurrence of this condition and absent efficacy data; since there are safety concerns with steroids, the use of steroids to treat Purtscher’s retinopathy is not currently advised.

References

1.Atabay C, Kansu T, Nurlu G (1993) Late visual recovery after intravenous methylprednisolone treatment of Purtscher’s retinopathy. Ann Ophthalmol 25:330 – 333

2.Blodi B, Johnson MW, Gass JDM, Fine SL, Joffe LM (1990) Purtscher’s-like retinopathy after childbirth. Ophthalmology 97:1654 – 1659

3.Burton TC (1980) Unilateral Purtscher’s retinopathy. Ophthalmology 87:1096 – 1105

4.Cooper BA, Shah GK, Grand MG (2004) Purtscher’s-like retinopathy in a patient with systemic lupus erythematosus. Ophthalmic Surg Lasers Imaging 35(5):438 – 439

5.Gass JDM (1987) Stereoscopic atlas of macular diseases: diagnosis and treatment. St. Louis, Mosby, pp 452 – 455

6.Jaco HS, Goldstein IM, Shapiro I, Craddock PR, Hammerschmidt DE, Weissmann G (1981) Sudden blindness in acute pancreatitis: possible role of complement-induced retinal leukoembolization. Arch Intern Med 141(1):134 – 136

7.Jacob HS, Craddock PR, Hammerschmidt DE, Moldow CF (1980) Complement-induced granulocyte aggregation: an unsuspected mechanism of disease. N Engl J Med 302:89 – 794

8.Kelley JS, Hartranft CD (2001) Traumatic chorioretinopathies. In: Ryan SJ, Schachat AP (eds) Retina. Mosby, St. Louis, pp 1815 – 1817

9.Lai JC, Johnson MW, Martonyi CL, Till GO (1997) Comple- ment-induced retinal arteriolar occlusions in the cat. Retina 17(3):239 – 246

10.Marr WG, Marr EG (1962) Some observations on Purtscher’s disease: traumatic retinal angiography. Am J Ophthalmol 54:693 – 705

11.Purtscher O (1910) Noch unbekannte Befunde nach Schadeltrauma. Berl Dtsch Ophthal Ges 36:294 – 301

12.Roden D, Fitzpatrick G, O’Donoghue H, Phelan D (1989) Purtscher’s retinopathy and fat embolism. Br J Ophthalmol 73:677 – 679

13.Wang AG, Yen MY, Liu JH (1998) Pathogenesis and neuroprotective treatment in Purtscher’s retinopathy. Jpn J Ophthalmol 42:318 – 322

Core Messages

Terson syndrome (Terson’s syndrome, Tersons syndrome) is defined as vitreous hemorrhage secondary to subarachnoid or subdural hemorrhage (Fig. 24.2.1). Subarachnoid bleeding is the more common cause

The less common subdural hemorrhage is often associated with brain trauma and permanent neurological or mental disability

Screening of patients with subarachnoid or subdural hemorrhage through the dilated pupil should be part of these patients’ management protocol

Presence of intraocular hemorrhage in patients with subarachnoid hemorrhage is a statistically significant risk factor for coma as well as for death

The vitreous hemorrhage may take months to spontaneously improve, but observation is not

without risks: proliferative vitreoretinopathy (PVR) can develop, leading to irreversible loss of vision

In approximately 40 % of patients with Terson syndrome, a hemorrhagic cyst (HMC) is found in the macular area. In approximately twothirds of these cysts, the blood is located under the internal limiting membrane (ILM) (submembranous HMC)

Treatment is aimed at removal of the intravitreal blood and evacuation of the cyst contents to hasten visual rehabilitation and to prevent blood-related complications

The timing of vitrectomy is primarily determined by the patient’s needs and wishes, but early intervention should be considered for eyes without spontaneous signs of blood resorption

Fig. 24.2.1. Fresh macular hemorrhage (submembranous HMC) in an eye with Terson syndrome after subarachnoid bleeding; the vitreous hemorrhage has already been removed

24.2.1 History

Although named after Terson, who described vitreous hemorrhage in association with spontaneous subarachnoid hemorrhage in 1900 [29], intraocular hemorrhage resulting from subarachnoid hemorrhage was first reported 19 years earlier by Litten [10]. Terson published additional observations on the condition in 1926 [30]. Intraocular hemorrhage following subdural hemorrhage (SDH) was first reported by McDonald in 1931 [14]. Intracranial pressure rise from causes other than hemorrhage (e.g., epidural saline injection) has also been reported to lead to Terson syndrome [21].

24.2.2Pathophysiology and Pathoanatomy

24.2.2.1 The Origin of the Intraocular Blood

directly originate from the subarachnoid space [1], entering the globe through the lamina cribrosa [31]. This could hardly explain, though, how subdural blood gets access to the globe.

A much more likely hypothesis is the sudden rise of intracranial pressure due to the extra fluid volume resulting from the extravasating blood. This in turn

24 III causes blockage and thus intraluminal pressure elevation in the venous channels draining blood from the globe. Consequent centrifugal rise in the venous pressure is immediate, and rupture of any of the veins inside the eye may then follow [33].

A third option would be partial or complete stasis in the central retinal vein, caused by transmission of the elevated intracranial pressure via the intravaginal spaces of the optic nerve sheath [5].

24.2.2.2The Type and Location of the Intraocular Blood

Since the pressure is elevated in each distal vein, hemorrhage can occur anywhere [12]: within the sheath of the optic nerve, in the orbit, and, most importantly, intraocularly. The blood inside the globe can appear in one or multiple locations:

Subretinal (Fig. 24.2.2)

Intraretinal

Preretinal (subhyaloidal; Fig. 24.2.3)

Intravitreal (Terson syndrome; Fig. 24.2.4)

The intraretinal hemorrhage can be in the deep layers or superficially, under the internal limiting membrane (ILM).

24.2.2.2.1Blood Accumulation in the Macular Area: Hemorrhagic Macular Cyst

The rapidity of visual rehabilitation depends to a great extent on whether a hemorrhagic macular cyst

(Fig. 24.2.5) also develops. Based on the exact location of the accumulated blood, two types of hemorrhagic cyst (HMC) are distinguished [19]:

Submembranous HMC (Fig. 24.2.1): the blood is located under the ILM; therefore it is an intraretinal bleeding

Preretinal HMC (Fig. 24.2.3): the blood is located in front of the ILM; therefore this is a subhyaloidal bleeding

The cyst can demonstrate various appearances, depending on its age:

A fresh HMC contains blood; therefore it is red (Fig. 24.2.6)

If degeneration of the blood has already started, the cyst appears white (Fig. 24.2.7)

Fig. 24.2.2. Subretinal blood accumulation in an eye following spontaneous clearing of the vitreous hemorrhage after subarachnoid bleeding

Fig. 24.2.3. Subhyaloidal hemorrhage (preretinal HMC) in a patient with Terson syndrome

Fig. 24.2.4. Typical appearance of vitreous hemorrhage in a patient with Terson syndrome

Fig. 24.2.5. Artist’s rendering of an HMC in a patient with Terson syndrome. The blood is already in the process of degenerating; hence the HMC’s whitish color. The rest of the fundus looks normal

III 24

Fig. 24.2.8. Intraoperative image of a submembranous HMC in an eye with Terson syndrome. The condition is several months old; the blood has completely absorbed, leaving clear fluid behind. Within a few weeks this fluid also gets absorbed, leaving behind a collapsed anterior cyst wall (ILM) in the form of surface wrinkling

Fig. 24.2.6. Intraoperative image of a submembranous HMC in an eye with Terson syndrome. The condition is fresh, the blood is still red

Fig. 24.2.7. Intraoperative image of a submembranous HMC in an eye with Terson syndrome. The condition is a few months old; the blood is partially absorbed already; the remaining blood has turned white

If the blood breakdown process is complete, the cyst may still contain clear fluid and appear transparent (Fig. 24.2.8)

The anterior wall of a submembranous cyst may collapse; its surface may be wrinkled and misdiagnosed as an epiretinal proliferation. In reality it is the nonelastic [7] ILM that has been permanently stretched by the blood

24.2.3 Epidemiology

The prevalence of intracranial aneurysm can be as high as 4.8 % [22]; however, most of those affected will not develop actual subarachnoid bleeding [34]. The incidence among those 25 years and older was 13.3 per 100,000 in men and 24.4 per 100,000 in women in a Swedish study; interestingly, during the

16years of observation, the age-standardized incidence in the 25 – 74 years group decreased significantly in men but remained essentially unchanged in women.

The largest prospective study [3] to date on patients surviving subarachnoid bleeding found that

17% developed some type of intraocular hemorrhage; the rate of Terson syndrome was 7 %. Other studies found intraocular hemorrhage rates up to

40% and vitreous hemorrhage rates up to 27 % [2, 3, 12, 23, 27, 35]. It must be noted that the figures underestimate the true incidence because they do not take into consideration people who die before they could have been examined, and mortality rates keep falling [28].

The largest study to date on eyes undergoing vitrectomy for Terson syndrome [9] found that 39 % of them had HMC (Figs. 24.2.1, 24.2.3, 24.2.5 – 24.8).

24.2.4 Significance

24.2.4.1Natural History of Vitreous Hemorrhage in Eyes with Terson Syndrome

Even without surgery, eyes with Terson syndrome 24 III generally have a good outcome: in most cases, the blood absorbs spontaneously. It must be noted, however, that complications are not rare with only observation – and today it appears that these complications may outweigh the risks of surgery. Complica-

tions include the following:

Epiretinal membrane formation in 75 % [25] Development of myopia (incidence unknown) [16]

Amblyopia in the appropriate age group [4] Retinal detachment (incidence unknown) [15] Proliferative vitreoretinopathy (PVR) (incidence unknown) [32]

24.2.4.2 Systemic Significance

The prognosis for patients sustaining subarachnoid hemorrhage has significantly improved, with a 40 % survival rate in the mid 1940s [11] to around 80 % today [6]. Nevertheless, the presence of vitreous hemorrhage remains an important prognostic sign. In various studies, the mortality rate for patients with subarachnoid hemorrhage is shown to be two to four times higher if Terson syndrome was also present [13, 26]. In one prospective study [3], 100 % of patients with Terson syndrome developed coma, as opposed to a 46 % rate in patients without vitreous hemorrhage, a statistically significant difference.

24.2.4.3 Human Significance

For most patients with Terson syndrome, especially for those in whom extensive brain damage is also present, visual rehabilitation is a key in achieving improvement in their quality of life. Persons with bilateral vitreous hemorrhage – 22 % of patients in Kuhn’s study [9] – are completely deprived of sight. Early restoration of vision greatly contributes to the well-being of the individual, family, and society; this must be taken into account when the choice between observation versus surgical intervention is contemplated (see under Sect. 24.2.6.1).

Fig. 24.2.9. Since the ILM is not elastic, its fluidic separation from the rest of the retina by the blood exerts traction along the circumference of the cyst as the ILM reinserts. Visibility of this fold (“macular ring”), appearing as a white line, is proportional with ILM elevation, e.g., the height of the accumulated blood

24.2.5 Diagnosis*

Patients with intracranial hemorrhage typically are first seen by a neurologist or neurosurgeon, although occasionally no neurological symptoms are present [20]. Screening of all patients with subarachnoid or subdural bleeding should be the norm [9]. It must be noted that mental problems are not rare in patients with intracranial hemorrhage; therefore they may not be able to communicate that their vision has dropped.

An ophthalmoscope is all that is needed to recognize that vitreous hemorrhage is present. In case of media opacity or if the pupil cannot be adequately dilated, ultrasonography may be necessary.

If there is no vitreous hemorrhage present, it must be noted whether other symptoms such as optic disc edema, flamed and dot-like intraretinal, or subretinal hemorrhages have occurred.

Accumulation of blood in the macular area (HMC) is almost pathognomic.

A retinal fold (“macular ring,” Fig. 24.2.9) may be seen at the reinsertion of the detached ILM in eyes with a submembranous HMC [8].

It is very important in young children to verify whether child abuse has caused the subdural bleeding. Intraocular hemorrhages, however, do not necessarily point to child abuse.

24.2.5.1 Differential Diagnosis

Vitreous hemorrhage of other etiologies should be excluded.

24.2.6 Treatment*

24.2.6.1 Indication and Counseling

Typically, ophthalmologists use an artificially determined visual acuity value (e.g., 20/200) or duration (e.g., 3 months) to decide whether they recommend further observation or surgical intervention. Not only does this approach have no scientific basis, it completely ignores the patient’s individual needs. Some people are more keen than others to hasten visual recovery because of personal or professional reasons; others would rather wait even if the condition is bilateral.

A careful, personalized approach is the most optimal option. The ophthalmologist should discuss the advantages and disadvantages of observation as well as those of surgery, and help the patient – or, in case of a minor or a mentally disabled patient, the family – to make the decision [17]. It is important to emphasize that delaying surgery has its own complications (see above) and that the risk of serious, vitrectomy-related complications is low. Early surgery should therefore definitely be considered [24] with the patient (guardian) having the final say.

*Only the ophthalmic aspects are covered here; for the neurosurgical treatment (Fig. 24.2.10), the reader is referred to the appropriate textbooks.

24.2.6.2 Surgery

The only intervention proven to be effective for vitreous hemorrhage is vitrectomy.

Fig. 24.2.10. Intraoperative image of clipping of the aneurysm during neurosurgery

Fig. 24.2.11. Intraoperative image showing removal of the ILM in an eye with submembranous HMC. Degenerated blood products are still visible as is the retinal fold shown in Fig. 24.2.9

24 III

Fig. 24.2.12. Postoperative image of an eye that underwent ILM removal for submembranous HMC in a patient with Terson syndrome. The eye has maintained full vision after a follow-up exceeding 13 years. In this young individual, the shiny reflex from the area without ILM removal clearly delineates it from the central, ILM-deprived area

Infrequent postoperative complications include retinal detachment with or without PVR, and epiretinal proliferation if the ILM has not been removed [36]. The rate of postoperative epiretinal proliferation occurrence is less than in nonvitrectomized eyes. Cataract is inevitable in phakic patients, although their development may be delayed for decades in young patients. No adverse effect caused by ILM removal is expected, even during long-term follow-up (Fig. 24.2.12) The prognosis is poor in children, due to concurrent brain damage [9]

24.2.6.4 Follow-up

Other than cataract, complications are not expected to occur once the patient is past the traditional 6- month follow-up. Long-term care, involving psychiatrists, neurologists, physical therapists, social workers, etc., may be necessary for people with nonophthalmological disabilities.

24.2.7 Summary

Screening of patients with acute intracranial bleeding should be performed to allow early recognition of vision-threatening intraocular hemorrhages. Once the diagnosis of Terson syndrome is made, surgery to remove the blood and the often present hemorrhagic macular cyst should be considered. Vitrectomy probably has fewer side effects than long-term observation, and hastens visual rehabilitation in these patients, who commonly have to face other consequences of the intracranial hemorrhage.

References

1.Castano-Duque C, Pons-Irazazabal L, Lopez-Moreno J (1997) Subarachnoid hemorrhage associated to subhyaloid hemorrhage: Terson syndrome. Rev Neurolog 25:1081 – 1083

2.Fahmy JA (1973) Fundal haemorrhages in ruptured intracranial aneurysms I. Material, frequency, and morphology. Acta Ophthalmol 51:289 – 298

3.Frizzel R, Kuhn F, Morris R, Quinn C, Fisher W (1997) Screening for ocular hemorrhages in patients with ruptured cerebral aneurysms: A prospective study on 99 patients. Neurosurgery 41:529 – 534

4.Greenwald MJ, Weiss A, Oesterle CS, Friendly DS (1986) Traumatic retinoschisis in battered babies. Ophthalmology 93:618 – 625

5.Hayreh S, Edwards J (1971) Ophthalmic arterial and venous pressures: effects of acute intracranial hypertension. Br J Ophthalmol 55:649 – 663

6.Ikawa F, Ohbayashi N, Imada Y, Matsushige T, Kajihara Y, Inagawa T, Kobayashi S (2004) Analysis of subarachnoid hemorrhage according to the Japanese Standard Stroke Registry Study – incidenc, outcome, and comparison with the International Subarachnoid Aneurysm Trial. Neurol Medico-Chirurg 44:275 – 276

7.Kuhn F (2003) Internal limiting membrane removal for macular detachment in highly myopic eyes. Am J Ophthalmol 135:547 – 549

8.Kuhn F, Morris R, Mester V (2000) Macular rings in Terson’s syndrome. Acta Ophthalmol 78:721 – 722

9.Kuhn F, Morris R, Mester V, Witherspoon C (1998) Terson’s syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. Ophthalmology 105:472 – 477

10.Litten M (1881) Über einige vom allgemein-klinischen Standpunkt aus interessante Augenveränderungen. Berl Klin Wochnschr 18:23 – 27

11.Manschot W (1944) The fundus oculi in subarachnoid hemorrhage. Acta Ophthalmol 22:281 – 299

12.Manschot W (1954) Subarachnoid hemorrhage: intraocular symptoms and their pathogenesis. Am J Ophthalmol 38:501 – 505

13.McCarron M, Alberts M, McCarron P (2004) A systematic review of Terson’s syndrome: frequency and prognosis after subarachnoid haemorrhage. J Neurol Neurosurg Psych 75: 491 – 493

14.McDonald A (1931) Ocular lesions caused by intracranial hemorrhage. Trans Am Ophthalmol Soc 29:418 – 432

15.McRae M, Teasell R, Canny C (1994) Bilateral retinal detachments associated with Tersons syndrome. Retina 14:467 – 469

16.Miller-Meeks MJ, Bennett SR, Keech RV, Blodi CF (1990) Myopia induced by vitreous hemorrhage. Am J Ophthalmol 109:199 – 203

17.Morris R, Kuhn F, Witherspoon C (1988) Counseling the eye trauma victim. In: Alfaro V, Liggett P (eds) Vitrectomy in the management of the injured globe. Lippincott Raven, Philadelphia, pp 25 – 29

18.Morris R, Kuhn F, Witherspoon C (1994) Retinal folds and hemorrhagic macular cysts in Terson’s syndrome. Ophthalmology 101:1

19.Morris R, Kuhn F, Witherspoon C, Mester V, Dooner J (1997) Hemorrhagic macular cysts in Terson’s syndrome and its implications for macular surgery. Dev Ophthalmol 29:44 – 54