Chapter 141 – Distant Trauma with Posterior Segment Effects
CARL D. REGILLO
Shaken Baby Syndrome
• Intraocular hemorrhage associated with acute intracranial hemorrhage.
• Bilateral, multiple posterior segment hemorrhages.
• Intraretinal, preretinal, or intravitreal location.
• Spontaneous or trauma-induced intracranial blood (usually subarachnoid).
• Decreased vision with good spontaneous recovery.
• Peripapillary retinal infarctions associated with severe trauma or various systemic conditions (e.g., acute pancreatitis).
• Bilaterally symmetrical peripapillary cotton-wool spots.
• Bilateral retinal hemorrhages.
• Severe head, chest, or long bone injury.
• Amniotic fluid embolism.
• Other rare systemic conditions.
• Decreased vision with variable or limited recovery.
• Intraocular hemorrhage that results from whiplash-like child abuse.
• Bilateral retinal or vitreous hemorrhage.
• No evidence for direct eye trauma.
• Intracranial hemorrhage (usually subdural).
• Cerebral edema or atrophy.
• Decreased vision.
• Variable recovery as a result of ocular or central nervous system damage.
In 1900, Terson reported the association of vitreous hemorrhage with an acute subarachnoid hemorrhage. The syndrome that now bears his name, however, has evolved to include cases with any type of intraocular hemorrhage present after spontaneous or trauma-induced intracranial bleeding.
EPIDEMIOLOGY AND PATHOGENESIS
Intraocular hemorrhage is seen in approximately 20% of patients with acute intracranial bleeding.  Significant vitreous hemorrhage occurs in a smaller percentage of these patients, being observed with an incidence of 3–5% of all patients who have intracranial bleeding. The intracranial hemorrhage can be subdural, subarachnoid, or intracerebral in location. Subarachnoid bleeding from a cerebral aneurysm, in particular an aneurysm of the anterior communicating artery, is the most common underlying cause.
The pathogenesis of Terson’s syndrome has been a controversial subject for many years. Some investigators, early on, assumed that the intraocular hemorrhage resulted from direct dissection of the subarachnoid hemorrhage down the optic nerve sheath and into the eye. The lack of communication between the subarachnoid space of the optic nerve and the vitreous renders this mechanism unlikely. Furthermore, the retinal hemorrhages are often not contiguous with the optic nerve and autopsy studies have not shown that the optic nerve sheath hemorrhage extends to the globe.
It is believed now that the sudden rise in intracranial pressure that occurs at the time of the intracranial bleed is the primary event that leads to intraocular bleeding. In support of this theory is the observation that the amount of ocular hemorrhage correlates directly with the rapidity and magnitude of intracranial pressure elevation. How increased intracranial pressure translates into intraocular bleeding remains unclear. Increased orbital venous pressure translated directly through the cavernous sinus or compression of both the ophthalmic vein and adjacent retinochoroidal anastomoses—because of a rapid effusion of cerebrospinal fluid or of blood into the optic nerve sheath—could explain the phenomenon.    In either scenario, an acute obstruction to the retinal venous circulation results and leads to the rupture of superficial retinal vessels.
Terson’s syndrome consists of multiple, usually bilateral, retinal hemorrhages in the posterior pole (see Fig. 141-1 ). Visual acuity is often diminished, but this may not be easily quantified when the neurological manifestations predominate. The amount of acute vision loss is typically related to the extent of ocular hemorrhage.
Figure 141-1 Terson’s syndrome. Multiple superficial intraretinal hemorrhages and preretinal hemorrhage in an eye of a patient who had suffered intracranial bleeding from head trauma. (Courtesy of Lon S. Poliner, MD.)
Differential Diagnosis of Terson’s Syndrome
Shaken baby syndrome
Although hemorrhages can be subretinal and deep intraretinal in location, they are usually more superficial, being just under the internal limiting membrane or preretinal (subhyaloid). Significant vitreous hemorrhage is possible, probably from intraretinal blood that breaks through the internal limiting membrane or posterior hyaloid face into the vitreous gel. Late complications include epiretinal membrane formation, perimacular retinal folds, and, rarely, traction or rhegmatogenous retinal detachments. 
DIAGNOSIS AND ANCILLARY TESTING
The typically devastating consequences of acute intracranial hemorrhage, rather than the intraocular consequences, bring the patient to seek medical attention. In such patients, the diagnosis of Terson’s syndrome is generally obvious on initial ophthalmic evaluation. It may be an important diagnosis to establish as some series suggest that the presence of intraocular hemorrhage in this setting may be associated with a higher mortality than when no ocular involvement occurs. In suspected cases without established intracranial hemorrhage, emergency neuroimaging with either tomography or magnetic resonance imaging is indicated.
The differential diagnosis for Terson’s syndrome is given in Box 141-1 .
TREATMENT AND OUTCOME
In Terson’s syndrome, the blood typically clears completely and the visual acuity returns to normal.  However, in some cases the vision remains decreased from persistent vitreous hemorrhage or epiretinal membrane formation. In such situations, vitrectomy to clear the hemorrhage or remove membranes can improve the visual outcome.  The rare, associated retinal detachment requires surgical intervention. Even in cases without these significant complications, occasionally some degree of visual acuity loss may persist indefinitely because subretinal hemorrhage has resulted in disruption of the retinal pigment epithelium or direct damage to the outer retina in the foveal area.
In 1910, Purtscher described the occurrence of bilateral patches of retinal whitening and hemorrhage around the optic disc in patients who suffered massive head trauma. Subsequently, this fundus appearance was observed to be associated with other types of trauma, along with a variety of nontraumatic systemic diseases such as acute pancreatitis, systemic lupus erythematosus, thrombotic thrombocytopenic purpura, and chronic renal failure.   
EPIDEMIOLOGY AND PATHOGENESIS
There are both clinical and experimental data to suggest that Purtscher’s retinopathy results from the occlusion of small arterioles by intravascular microparticles generated by the underlying systemic condition.    These microparticles may consist of fibrin clots, platelet-leukocyte aggregates, fat emboli, air emboli, or other particles of similar size that block the arterioles in the peripapillary retina. It has been shown experimentally that fibrin clots 0.15–1.0?mm in size injected into the ophthalmic artery of pigs can produce a fundus appearance that mirrors Purtscher’s retinopathy.
Subjectively, patients experience acute, painless, loss of central vision in one or both eyes. The visual acuity loss is often marked. Ophthalmoscopy reveals multiple, variably sized cotton-wool spots and intraretinal hemorrhages around the optic nerve head ( Figs. 141-2 and 141-3 ). Some degree of asymmetry is often seen, but a unilateral picture is rare. Acutely, the optic nerve head and peripheral retina are usually of normal appearance, although commonly the disc exhibits pallor over time ( Fig. 141-3 , B).
DIAGNOSIS AND ANCILLARY TESTING
Classically, Purtscher’s retinopathy occurs in conjunction with severe head or chest trauma. It can also be seen after extensive fracture injury of long bone. For trauma-related cases, the diagnosis is apparent after fundus examination and no further evaluation is needed. However, for cases associated with a systemic medical condition, the underlying cause may not be readily recognizable by either patient or physician. Such patients may present to the ophthalmologist first if the ocular symptoms predominate. Therefore, the fundus appearance of Purtscher’s retinopathy without a history of recent trauma or an already known causative medical condition requires a comprehensive medical evaluation performed in conjunction with an internist. Fluorescein angiography shows areas of capillary dropout corresponding to the patches of retinal whitening and blocked fluorescence from intraretinal blood. Angiographic evidence for a lack of retinal capillary around the fovea may be present in cases with decreased visual acuity.
Systemic conditions associated with Purtscher’s retinopathy are listed in Box 141-2 .
Figure 141-2 Purtscher’s retinopathy. Near-confluent cotton-wool spots clustered around an otherwise normal optic nerve head in an eye of a patient who had sustained a severe blunt injury to the head and chest. (Courtesy of Jeffrey G. Gross, MD.)
Histopathologically, evidence exists for retinal capillary obliteration and inner retinal atrophy in areas of clinically observed retinal whitening. These findings are relatively nonspecific, being consistent with cotton-wool spots of a variety of causes. As noted clinically, the pathology is confined mainly to the retina posterior to the equator. Optic atrophy is typically present to various degrees.
TREATMENT AND COURSE
No known treatment exists for Purtscher’s retinopathy. Although retinal whitening and retinal hemorrhages slowly disappear over weeks or months, usually no significant recovery of vision occurs. The visual acuity remains decreased on the basis of infarction of either the foveal retina or optic nerve. Macular pigmentary alterations and optic atrophy are typical late findings. Medical or surgical therapy directed at the underlying condition, however, should help to prevent additional retinal or optic nerve damage by eliminating or reducing the potential for new emboli to form.
SHAKEN BABY SYNDROME
In the 1970s, the radiologist John Caffey proposed a whiplash-like mechanism of child abuse to explain the association of ocular and intracranial bleeding in infants who lacked external signs of direct head trauma. These are now recognized as hallmark findings of the shaken baby syndrome. Unfortunately, this syndrome represents a common form of child abuse that often results in significant morbidity and mortality. As the name implies, it is encountered almost exclusively in children younger than 2 years of age, most of whom are younger than 12 months. 
EPIDEMIOLOGY AND PATHOGENESIS
The age predilection is thought to be due to certain anatomical features that make the infant more likely to suffer from intracranial and intraocular bleeding as a result of shaking. The head of an infant is proportionately larger and heavier relative to the body than that of an older child or adult and is not as well stabilized
Figure 141-3 Purtscher’s retinopathy associated with thrombotic thrombocytopenic purpura. (A, At presentation. B, After 4 months of follow-up. Peripapillary retinal whitening and hemorrhage slowly resolved to leave macular pigment mottling and optic disc pallor. Visual acuity remained unchanged in the counting fingers range. (Copyright 1997, American Medical Association. With permission from Power MH, Regillo CD, Custis PH. Thrombotic thrombocytopenic purpura associated with Purtscher retinopathy. Arch Ophthalmol. 1997;115:128–9.)
Systemic Conditions Associated with Purtscher’s Retinopathy
Severe head, chest, or long bone trauma
Systemic lupus erythematosus (SLE)
Fat embolism syndrome
Thrombotic thrombocytopenic purpura (TTP)
Chronic renal failure
Amniotic fluid embolism
by neck muscles. The average adult is also able to generate relatively larger acceleration-deceleration forces when shaking an infant than when shaking a larger person.
Intracranial bleeding in this setting is believed to result primarily from the delicate vessels that bridge the cerebral cortices and venous sinuses being torn when the brain quickly shifts within the cranium during the forceful shaking. Direct contusion effects probably also occur. Blood, edema, and intracranial pressure elevation all play a role in the often permanent neurological damage.
The pathogenesis of the ocular hemorrhage is not as well understood. Although a mechanism akin to that of Terson’s syndrome may be a possible explanation, it is likely that the movement of the vitreous gel within the globe contributes to secondary traction on the internal limiting membrane and superficial retinal vessels. Increased venous pressure transmitted to the retina, such as in Valsalva retinopathy, may also occur, especially with a firm grip on the chest with shaking or even from direct choking of the victim.
The most common ocular finding in shaken baby syndrome is intraocular hemorrhage in various locations—subretinal, intraretinal, preretinal (subhyaloid), and intravitreal.     Intraretinal and preretinal hemorrhages predominate ( Fig. 141-4 ). As in Terson’s syndrome, the hemorrhages are concentrated in the posterior pole region and are usually bilateral. In many cases, the amount of intraocular blood correlates with the degree of acute neurological damage. Cotton-wool spots, white-centered hemorrhages, macular edema, papilledema, and retinoschisis are less common findings at presentation.  After the abuse has stopped, hemorrhages and other acute changes resolve within several months. Late manifestations include perimacular retinal folds, chorioretinal atrophy or scarring, optic atrophy, and retinal detachment.  
DIAGNOSIS AND ANCILLARY TESTING
The diagnosis of shaken baby syndrome is made when the ocular findings just discussed are present in conjunction with certain systemic features and a history of shaking abuse. As a history of physical abuse may be difficult or impossible to elicit with certainty, especially at first, the clinician must maintain a high index of suspicion based on the constellation of clinical findings. The hallmark nonocular sign in shaken baby syndrome is intracranial hemorrhage. Unlike that in Terson’s syndrome, this is usually subdural in location and often involves both sides
Figure 141-4 Shaken baby syndrome. Numerous superficial retinal hemorrhages (many with white centers) in the posterior pole of an infant who had been the subject of shaking abuse. (Courtesy of Dennis P. Han, MD.)
of the brain.   Other intracranial findings include subarachnoid or intracerebral blood, cerebral edema, and cerebral atrophy. Elevated intracranial pressure is often present. A variety of neurological symptoms, ranging from irritability and lethargy to seizures, coma, and death, can occur. Neuroimages from computed tomography or magnetic resonance imaging are utilized to diagnose the intracranial pathology. Cerebrospinal fluid and subdural aspirations may be needed in selected cases to confirm the presence of blood in the central nervous system.
Extracranial signs of abuse may also be evident and help confirm the diagnosis. From shaking injury alone, bruises or fractures that involve the trunk or limbs can be seen. Cervical cord hematomas have also been described and are thought to be strongly suggestive of whiplash-like injury. However, with shaking as the only mechanism of abuse, there is often a paucity of overt extracranial findings.
Intraocular hemorrhages in infancy, although highly indicative of shaken baby syndrome, are not specific for child abuse as they can be seen in a variety of other conditions during infancy ( Box 141-3 ). Direct trauma to the head or a spontaneous subarachnoid hemorrhage can result in intraocular bleeding, as described in the section on Terson’s syndrome. Retinal hemorrhages can also be seen after vaginal delivery and cardiopulmonary resuscitation. Finally, a number of systemic conditions, such as arterial hypertension, hematological disorders (e.g., leukemia), sepsis, meningitis, and vasculitis, can cause various degrees of intraretinal hemorrhage.
As observed clinically, the most common histopathological finding is intraocular hemorrhage with the blood observed in all layers of the retina, between the retina and the retinal pigment epithelium (RPE), and in the vitreous.  Intraorbital optic nerve sheath hemorrhage with blood is observed frequently and may cause or contribute to optic disc edema or optic atrophy.   Intraretinal edema, retinal folding, and RPE alterations are other, not uncommon, ocular findings. Other pathological changes of the globe are unusual in a case of shaken baby syndrome alone.
TREATMENT, COURSE, AND OUTCOME
Some degree of permanent visual loss is common in shaken baby syndrome, and, therapeutically, little can be done to alter the visual outcome. Irreversible damage to the macula, optic nerve, occipital cortex, or some combination of these is responsible for the decreased vision.    Signs indicative of at least a fair potential for visual function are good pupillary reflexes, clear ocular media, retinal findings that are limited to intraretinal hemorrhages, and a normal optic nerve head. In patients who have vitreous hemorrhage dense enough to obscure the
Causes of Retinal Hemorrhages in Infancy
Birth trauma (neonates only)
Shaken baby syndrome
Spontaneous intracranial hemorrhage (Terson’s syndrome)
Direct eye, head, or chest trauma (accidental or nonaccidental)
Systemic infections and meningitis
Hematologic disorders (e.g., malignancies, coagulopathies)
Systemic (or retinal) vasculitis
macula, vitrectomy surgery to clear the blood can be performed. In this setting, electroretinography should be utilized preoperatively as surgery is not likely to be of benefit if there is no significant bright flash response. Unfortunately, although the visual pathway may be relatively well preserved, the patient’s overall function may still be very limited as a result of severe neurological damage.
A whiplash injury to the head in adults produces a unique ocular problem referred to as whiplash maculopathy. In this disorder, the patient usually reports bilateral, mild blurring of vision that begins immediately after a significant head and neck flexion-extension injury. Automobile accidents with rapid deceleration are the most common cause. Visual acuity is found to be slightly decreased, rarely worse than 20/30, and ocular examination is notable only for a faint gray haze to the foveal retina accompanied by a small depression. A shallow posterior vitreous separation may also be seen. Fluorescein angiography is usually normal. Within days, the vision returns to normal and the gray retinal discoloration fades, but the small, foveal depression appears to persist indefinitely. Similar foveal changes can be seen after direct eye trauma with mild commotio retinae of the central macula and after sun gazing (solar retinopathy).
FAT EMBOLISM SYNDROME
Distinct posterior segment changes are also seen in the fat embolism syndrome. Within a few days of sustaining significant fractures of medullated bones, a variety of systemic and ocular signs can be manifest. Retinal changes are observed in as many as 60% of patients who meet the diagnostic criteria of fat embolism syndrome but in only about 5% of the patients who present with long bone fractures, with or without other systemic signs.
The classical eye findings are bilateral cotton-wool spots and intraretinal hemorrhages.  Although the syndrome may resemble Purtscher’s retinopathy, the white retinal infarcts and hemorrhages are usually smaller, less numerous, and more peripheral.  Moreover, it differs from Purtscher’s retinopathy in that most patients are either asymptomatic or have only minor visual complaints.
The associated systemic manifestations of fat embolism syndrome include petechial rash, central nervous system alterations, respiratory compromise, fever, tachycardia, anemia, and elevated erythrocyte sedimentation rate. The condition is fatal in 20% of cases. The ophthalmologist is rarely involved during the acute phase of fat embolism syndrome as ocular symptoms are usually minimal. However, some patients notice persistent paracentral scotomata and the ophthalmologist may be in a position to evaluate these and other ocular symptoms at some point during or after the acute phase of the syndrome. 
No treatment is currently available for ocular manifestations associated with fat embolism syndrome.
Valsalva retinopathy occurs when increased intrathoracic or intra-abdominal pressure is transmitted to the eye, which results in intraocular bleeding. The hemorrhage is usually unilateral or bilaterally asymmetrical and located in the macula. Subinternal limiting membrane hemorrhage is most common, but subretinal, retinal, and/or intravitreal bleeding can occur as well. Coughing, vomiting, sneezing, straining at stool, lifting, and sexual intercourse are all possible causes. Valsalva retinopathy typically clears without sequelae. The neodymium: yttrium-aluminum-garnet laser has been used to disrupt preretinal hemorrhage in selected cases to speed the clearance. In most cases, however, laser or surgical intervention is rarely ever needed.
1. Williams DF, Mieler WF, Williams GA. Posterior segment manifestations of ocular trauma. Retina. 1990;10:S35–S44.
2. Garfinkle AM, Danys IR, Nicolle DA, et al. Terson’s syndrome: a reversible cause of blindness following subarachnoid hemorrhage. J Neurosurg. 1992;76:766–71.
3. Ogawa T, Kitaoka T, Dake Y, Amemiya T. Terson syndrome. A case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology. 2001;108:1654–6.
4. Schultz PN, Sobol WM, Weingiest TA. Long-term visual outcome in Terson syndrome. Ophthalmology. 1991;98:1814–19.
5. Kuhn F, Morris R, Witherspoon CD, Mester V. Terson syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. Ophthalmology. 1998;105:472–7.
6. Gnanaraj L, Tyagi AK, Cottrell DG, et al. Referral delay and ocular surgical outcome in Terson syndrome. Retina. 2000;20:374–7.
7. Purtscher O. Angiopathia retinae traumatica. Lymphorrhagien des Augengrundes. Arch Ophthalmol. 1912;56:244–7.
8. Gass JDM. Stereoscopic atlas of macular disease: diagnosis and treatment, 3rd ed. St Louis: Mosby–Year Book; 1997:452–5, 746–7.
9. Power MH, Regillo CD, Custis PH. Thrombotic thrombocytopenic purpura associated with Purtscher retinopathy. Arch Ophthalmol. 1997;115:128–9.
10. Chuang EL, Miller FS, Kalina RE. Retinal lesions following long bone fractures. Ophthalmology. 1985;92:370–4.
11. Behrens-Baumann W, Scheurer G, Schroer H. Pathogenesis of Purtscher’s retinopathy: an experimental study. Graefes Arch Clin Exp Ophthalmol. 1992; 230:286–91.
12. Greenwald MJ. The shaken baby syndrome. Semin Ophthalmol. 1990;5:202–14.
13. Levin AV. Ocular manifestations of child abuse. Ophthalmol Clin North Am. 1990;3:249–64.
14. Kivlin JD. Manifestations of the shaken baby syndrome. Curr Opin Ophthalmol. 2001;12:158–63.
15. Munger CE, Peiffer RL, Bouldin TW, et al. Ocular and associated neuropathologic observations in suspected whiplash shaken infant syndrome: a retrospective study of 12 cases. Am J Forensic Med Pathol. 1993;14:193–200.
16. Riffenburgh RS, Sathyavagiswaran L. Ocular findings at autopsy of child abuse victims. Ophthalmology. 1991;98:1519–24.
17. McCabe CF, Donahue SP. Prognostic indicators for vision and mortality in shaken baby syndrome. Arch Ophthalmol. 2000;118:373–7.
18. Han DP, Wilkinson WS. Late ophthalmic manifestations of the shaken baby syndrome. J Pediatr Ophthalmol Strabismus. 1990;27:299–303.
19. Hadley MN, Sonntag VKH, Rekate HL, Murphy A. The infant whiplash-shake injury syndrome: a clinical and pathologic study. Neurosurgery. 1989;24:536–40.
20. Kelley JS, Hoover RE, George T. Whiplash maculopathy. Arch Ophthalmol. 1978; 96:834–5.