- Email: [email protected]
Traumatic Retinoschisis in Battered Babies
Traumatic Retinoschisis in Battered Babies MARK J. GREENWALD, MD, AVERY WEISS, MD, CAROLYN S. OESTERLE, MD, DAVID S. FRIENDLY, MD
Abstract: Five infants who were victims of physical abuse had extensive bilateral retinal hemorrhages on initial evaluation and subsequently developed signs of permanent retinal damage. None showed external evidence of trauma to the eyes. Vitreous hemorrhage developed after a delay of several days or more in three cases that were followed closely from the time of the traumatic incident. In several eyes, apparent intraretinal blood-filled cavities were seen acutely in the macular region and elsewhere. Late scarring of the macula typically had a cystic or crater-like configuration. Electroretinography showed loss or reduction of the positive B-wave with preservation of the negative A-wave in every case. We propose that splitting of the retina resulting from the direct mechanical effects of violent shaking was responsible for all of these findings. [Key words: battered baby syndrome, child abuse, electroretinogram, macular lesion, retinal hemorrhage, retinoschisis, shaking trauma, subdural hemorrhage, vitreous hemorrhage.] Ophthalmology 93:618-625, 1986
Numerous reports have documented the frequent occurrence of hemorrhages in the ocular fundi of infants who have been physically abused. 1 ~ 11 Subretinal, retinal, preretinal, subhyaloid, and vitreous hemorrhages have been described. In most cases these are bilateral, and typically periocular and anterior segment signs of trauma are absent, suggesting an etiology other than direct contusion of the globe. Very commonly there is associated intracranial hemorrhage, often without skull fracture or external signs of a blow to the head. Caffey and others have argued convincingly that such cases may result from violent manual shaking by an adult, with repeated whiplashing of the infant's inadequately supported headY· 13 The pathogenesis of intraocular hemorrhages in battered babies remains uncertain. Retinal and vitreous hemorrhages are found frequently in patients with intracranial bleeding of any etiology, probably in consequence of acute elevation of intracranial pressure. 14•15 Their occurrence has been documented in abused infants with neither blood nor elevated pressure intracranially, From the Departments of Ophthalmology, Children's Hospital National Medical Center, Washington, DC, Northwestern University Medical School, Chicago. Presented at an Annual Meeting of the American Academy of Ophthalmology. Reprint requests to Mark J. Greenwald, MD, Division of Ophthalmology, Children's Memorial Hospital, 2300 Children's Plaza, Chicago, IL 60614.
618
however. 7 Hemodynamic stresses generated by chest compression or by extreme forms of abuse such as swinging the child around by its feet have been invoked in such cases. 1•7 In some abused infants with fundus hemorrhages, complete resolution occurs, while in others significant permanent visual loss is observed in one or both eyes. 3•4 Optic atrophy is typically present in such cases. Scarring and cyst formation in the macula have been reported. Afferent pupillary defects and strabismic deviation of unilaterally affected eyes may occur. The nature of the process that causes chronic disturbances in the retina and the optic nerve and the sequence through which these changes develop from acute hemorrhagic retinopathy have received little attention. Retinal hemorrhages occurring in infants in other circumstances (eg. in newborns following vaginal delivery) virtually always resolve to leave the fundus completely normal. 16 We report five cases of children in whom definite or probable physical abuse during infancy was associated with the development of extensive fundus hemorrhages, and in whom permanent scarring and decreased vision resulted. The evolution of physical findings was observed over a period of months to years and the functional status of the retina was assessed by means of electroretinography in every case. The consistent occurrence of certain distinctive features in these patients appears to define a clinical entity that we have designated "traumatic retinoschi-
GREENWALD, et al •
sis." The pathophysiological meachanism of this syndrome may be quite unlike those of other hemorrhagic retinopathies.
CASE REPORTS Case 1. A 9-month-old black girl was admitted to the intensive care unit (ICU) because of stupor, seizures, and episodic apnea. She had undergone surgery for congenital esotropia at age seven months; her ocular examination at that time had been otherwise normal and her general condition unremarkable. One week prior to hospitalization she developed an upper respiratory infection. On the day of admission, while in the care of a babysitter, she reportedly vomited, had a seizure, and became unresponsive. No history of physical abuse could be elicited. On arrival in the ICU the child was markedly obtunded and showed decerebrate posturing. The pupils were nonreactive and retinal hemorrhages were noted bilaterally. There was no external or radiographic evidence of trauma. On chest x-ray there was a right upper lobe infiltrate. Computed tomography did not disclose any intracranial hematoma. Lumbar puncture gave an opening pressure of 360 mm; in cerebrospinal fluid, glucose and protein were normal and there were 6500 red blood cells and 25 white blood cells (87% mononuclear) per cubic millimeter. All bacterial cultures and viral titers (herpes, cytomegalovirus, Epstein-Barr virus) were negative. Sickle hemoglobin was not present in red blood cells. Ophthalmological evaluation on the third hospital day confirmed that the pupils did not react to light, but they did vary spontaneously from 3 to 5 mm in diameter. There was no sign of visual interest and the eyes were tonically deviated downward. External and anterior segment structures were unremarkable and the vitreous was perfectly clear. On fundus examination, the discs appeared normal. Scattered throughout both fundi, but concentrated in the posterior poles, were a number of lesions that appeared to be intraretinal blood-filled cavities, within which the red blood cells had partially layered out inferiorly (Fig 1). The largest of these were in the macular regions bilaterally, extending out as far as the major vascular arcades. There was extensive hemorrhage without cyst formation elsewhere in the retina and the nonhemorrhagic retinal areas appeared thickened, opaque, and grayish in both eyes. On reexamination one week later there was possibly slight arousal in response to bright light, but no definite pupillary response could be documented. In contrast to the previous examination, the vitreous was filled with blood bilaterally and the fundi could not be seen at all. The child recovered consciousness but was left with severe spastic quadriparesis, seizures, and profound mental retardation. Subsequent computed tomography showed marked diffuse cerebral atrophy. Six months after discharge from the hospital, repeat ophthalmological evaluation demonstrated perststent lack of response to visual stimulation and nonreactivity ofthe pupils. There had been almost complete clearing of the vitreous in both eyes. The retinal vessels were markedly narrowed and sclerotic and there appeared to be extensive gliosis of the retina. An electroretinogram showed little or no positive B-wave with relatively good preservation of the negative A-wave (Fig 2). Reevaluation, including electroretinography, one year later was essentially unchanged. The consensus among medical personnel was that physical abuse was the cause of this child's devastating condition, but after investigation by governmental authorities the family and the child's babysitter were exonerated.
TRAUMATIC RETINOSCHISIS
Case 2. An 8-month-old black boy was hospitalized in a deeply stuporous state following a succession of generalized seizures. His foster mother admitted having shaken him in an attempt to stop the seizures. The child, who was in the care of a family that was attempting to adopt him, had suffered seizure-like episodes since four months of age, according to the foster parents. A similar episode had led to hospitalization at age five months. On that occasion the infant was alert and showed normal visual behavior at the time of admission. Both pupils were normally reactive. Ophthalmological evaluation revealed clear media and multiple retinal and preretinal hemorrhages in the posterior pole of both eyes, with a pale appearance of the surrounding retina resembling Berlin's edema. Computed tomography demonstrated a small subdural hematoma on the left side, from which 10 cc of blood was aspirated. There were no signs of soft tissue injury or fractures. Developmental progress was normal for that age, and the child appeared well nourished. An electroencephalogram done several weeks after discharge showed spikes in the left parietal region consistent with a focal convulsive disorder. The family was investigated because of suspicion of child abuse and received a favorable assessment. At the time of readmission to the hospital the infant was responsive only to deep pain and showed signs of left hemiplegia. Computed tomography demonstrated bilateral subdural hematomas. Ophthalmological evaluation showed no evidence of responsiveness to visual stimulation. The pupils were both 6 mm in diameter and nonreactive to light. The eyes were divergent with marked limitation of rotation in response to vestibular stimulation. External and anterior segment structures were essentially normal. In both fundi there were noted to be extensive intraretinal and subretinal helmorrhages with a small amount of preretinal hemorrhage. The nonhemorrhagic portions of the retina appeared grayish and opaque. The discs were normal in appearance and the vitreous was clear. Two weeks after admission, reexamination disclosed that the vitreous had become filled with blood in both eyes, with almost complete obscuration of the fundi. The pupils remained nonreactive. An electroretinogram recorded one week later (with the vitreous still densely hemorrhagic) showed almost complete extinction of the B-wave with relatively good preservation of the A-wave in the right eye and a very low voltage response that was difficult to interpret in the left eye. The child remained hospitalized for one month. He recovered consciousness but remained hemiparetic and subsequently showed moderately severe mental retardation. Bilateral subdural-peritoneal shunts were required to prevent reaccumulation of subdural fluid. Ophthalmological reevaluation one year later again demonstrated the absence of any detectable visual function. The pupils were still completely nonreactive. A large angle exotropia was present with bilateral limitation of adduction. The vitreous hemorrhage had cleared bilaterally. Fundus examination showed marked narrowing of the retinal vessels and pallor ofboth discs. In the right macula there was a large intraretinal cyst or schisis cavity surrounded by a ring of apparent gliosis. In the left eye there was no discrete macular lesion but extensive gliosis was present in the posterior pole and vessels appeared to extend into the vitreous from the disc. During the second hospitalization, x-rays had disclosed a fracture of the left tibia. Reassessment of the family situation led to the child's being placed in a different home, and to criminal prosecution and conviction of the original foster mother. Case 3. A 10-month-old black girl sustained severe head trauma when she was assaulted by her babysitter's boyfriend. Prior to this she had been in good health and was developing
619
RE LE
RE
LE
620
Fig I. Top left. case I, right eye. Artist's rendering of acute fundus appearance. Fig 2. Middle lefi, case I. Electroretinogram recorded six
months after onset of retinopathy. Full field white flash , intensity 16 X 10 3 ft-L, duration 10 microseconds. Cornea positivity represented by upward deflection. Calibration symbol (lower right corner) represents 20 milliseconds horizontally and 100 microvolts vertically. Fig 3. Bottom /e.fi, case 4. Electroretinogram (ERG) recorded 2 1/2 months after onset of retinopathy. Both eyes had extensive retinal hemorrhages, but only the left had an impaired pupillary light response, delayed appearance of blood in the vitreous, and macular schisis. ERG parameters are the same as in Figure 2. Fig 4. Top right, case 5, right eye. Fundus appearance three years after onset of retinopathy. Fig 5. Bottom right. case 5, right eye. Electroretinogram recorded six years after onset of retinopathy. Parameters are the same as in Figure 2.
GREENWALD, et al •
normally. On arrival in the emergency room she was stuporous, responding only to pain. Both pupils were poorly reactive. Skull x-rays and computed tomography revealed a right occipital fracture and a large left subdural hemorrhage. The intracranial hematoma was evacuated acutely; it reaccumulated and a craniectomy with placement of drains was performed on the third day of hospitalization. Repeat computed tomography revealed a possible infarction of the brain in the distribution of the left posterior cerebral artery. One week after admission it was noted that the fundi could not be seen. Ophthalmological evaluation was performed on the 17th hospital day. There was a questionable blink response to bright light but both pupils were nonreactive at 5 mm diameter. External and anterior segment structures were unremarkable. Dense vitreous hemorrhage was present in both eyes; fundus details could barely be discerned. The child was discharged after nearly one month in the hospital alert and without focal neurologic deficits except for apparent blindness. Three months after injury there was still no definite evidence of any visual function and the pupils remained unresponsive to light. Only partial clearing of the vitreous hemorrhage had occurred; the fundi could still not be seen clearly, but B-scan ultrasonography demonstrated attached retinas. Electroretinography showed markedly diminished responses consisting only of initial negative potentials in both eyes. One year later, constant slow, roving, conjugate eye movements were noted. The right pupil was minimally reactive to direct light stimulation and the left pupil was completely nonreactive, showing a relative afferent defect. Vitreous hemorrhage had cleared entirely on the right and partially on the left to permit visualization of both fundi. The discs were pale and the vessels were markedly attenuated. Both retinas had a gliotic appearance, which was especially marked in a ring-shaped distribution surrounding the right macula, producing a crater-like appearance. The electroretinogram was repeated and showed essentially the same response noted previously. The child was last seen at age 4 years. Her intelligence was good. Profound visual impairment persisted, but light perception could be documented. Clearing of the vitreous hemorrhage was complete bilaterally. The appearance of the fundi was unchanged. Case 4. A 5-month-old white girl was hospitalized for seizures and obtundation. Her previous health and development had been normal. On the day of admission she had been irritable and sleepy. Late in the afternoon, while attended by a babysitter, she reportedly became rigid and unresponsive. No history of trauma or rough handling was obtained. The child was brought to the emergency room where tonic-clonic movements were observed. On admission she was lethargic and showed right hemiparesis with frequent brief episodes of right-sided jerking movements. The right pupil was normally reactive and the left was nonreactive. Retinal hemorrhages were noted bilaterally. Computed tomography showed a left subdural hemorrhage with a midline shift. There was no evidence of soft tissue injury or fractures. Ophthalmological consultation was obtained on the day after admission. Visual responsiveness could not be demonstrated. Vestibulo-ocular movements were intact. The right pupil reacted normally; the left showed no direct reaction but a normal consensual response (amaurotic pupil). External and anterior segment structures were normal and the vitreous was clear bilaterally. Multiple retinal and preretinal hemorrhages were present throughout the fundi, but concentrated in the posterior pole, and the nonhemorrhagic retina appeared edematous in both eyes. These abnormalities were more marked in the left eye. In addition, in the left eye only, a large dome-like elevation of the retinal surface in the posterior pole was observed, occupying most of the region within the temporal vascular arcades. The
TRAUMATIC RETINOSCHISIS
retina immediately surrounding this structure, which was described as retinoschisis, appeared thick and opague. On the tenth hospital day repeat eye examination showed no change in the pupils, with a persistent left afferent pupillary defect. In the right eye, the retinal hemorrhages had become smaller, the surrounding retina had recovered a nearly normal appearance, and the vitreous remained clear. On the left the vitreous had become filled with blood, which totally obscured the fundus. During two weeks of hospitalization the child was treated medically for cerebral edema and seizures but did not require surgery for her subdural hemorrhage, which resolved spontaneously. At discharge she was alert but had a mild persistent right hemiparesis. Reaccumulation of subdural fluid necessitated readmission for subdural-peritoneal shunt placement six weeks later. At that time ophthalmological evaluation showed normal fixation with the right eye and no fixation with the left. The pupils were unchanged from the first examination. The right fundus had recovered a completely normal appearance, while the left was still obscured by dense vitreous hemorrhage. B-scan ultrasonography demonstrated an attached retina in the left eye. The electroretinogram was normal on the right and on the left consisted only of the negative A-wave (Fig 3). The patient was last seen four months after the first hospitalization. Ocular findings were unchanged except for partial clearing of vitreous blood from the left eye. Although trauma was believed to be responsible for this child's condition, investigation of the case by governmental authorities did not lead to any action against the family. Case 5. A 2-month-old black boy was admitted to the hospital after being resuscitated by his father from an episode of apnea. The resuscitation measures had included shaking the baby as well as mouth to mouth ventilation, which was continued for an estimated ten minutes before spontaneous respiration returned. Prior to this the infant had been healthy except for the occurrence of a similar apneic spell two weeks earlier. In the emergency room he was noted to be alert and without focal neurological deficits. The right pupillary light reaction was impaired in comparison with the left. Retinal hemorrhages were observed bilaterally. Computed tomography demonstrated bilateral subdural hemorrhages. There were no other signs of trauma. The occurrence of apneic spells was documented during the period of hospitalization. After repeated reaccumulation of subdural fluid following aspiration, subdural-peritoneal shunts were placed bilaterally. The patient was discharged after three weeks. Ophthalmological consultation was not obtained during this hospitalization. The child was first seen in the eye clinic at age 7 months for evaluation of right esotropia, which had been noted by the family shortly after discharge from the hospital. Examination revealed poor fixation with the right eye and central steady maintained fixation with the left eye. Both pupils were reactive to light but an afferent defect was present on the right. Variable esotropia of moderate angle was present. External and anterior segment • structures were normal. There were fundus abnormalities bilaterally. On the right, the disc showed definite pallor, especially temporally. A large, elevated, apparently cystic lesion occupied the macula and the papillomacular area, surrounded by gliotic appearing retina. There was marked irregularity ofthe underlying retinal pigment epithelium. The disc appeared normal on the left but there was an unusual light reflection from the vitreoretinal interface and a mild disturbance of the retinal pigment epithelium. The retinal vessels were normal or slightly narrowed bilaterally. The child was followed for several years. His development progressed normally. Visual acuity at the last clinic visit was 20/ 400 in the right eye and 20/40 in the left. Findings on exami-
621
OPHTHALMOLOGY •
MAY 1986 •
nation remained approximately the same, except for some flattening of the cystic lesion in the right posterior pole (Fig 4). Strabismus correction was performed at age 3 years. An electroretinogram of acceptable quality was recorded six years after the traumatic episode. It showed reduction of the B-wave with an intact A-wave in both eyes (Fig 5). The hospital's child protection team investigated this case during the acute stage and concluded that the patient's injuries had resulted from unintentionally violent resuscitation measures performed by the father. No legal action was taken.
DISCUSSION All of the patients in our series came to medical attention during infancy, with ages ranging from 2 to 10 months. Three were girls and two were boys. Four of the five were black; the fifth was white. This racial distribution probably reflects the composition of the population that utilizes the hospital's emergency room. Subdural hemorrhages were present in four of our five cases, bilaterally in two. One of these children suffered major permanent brain damage; the other three recovered with only minor deficits aside from impaired vision. In the remaining case no intracranial hematoma was documented, but increased intracranial pressure was demonstrated acutely, and cerebral atrophy with severe neurological impairment developed subsequently. A skull fracture was present in only one patient, who was known to have been beaten. A fracture of the tibia was disclosed by a radiographic bone survey in another, who was believed to have been violently shaken. Clinical and laboratory evaluation failed to reveal any evidence of trauma other than ocular and central nervous system findings in the remaining three cases. A history of deliberate physical abuse was obtained in only one case. In two others a parent admitted having shaken the infant while trying to resuscitate it following loss of consciousness associated with a seizure or an apneic episode. In the remaining two cases the child was in the care of a babysitter when spontaneous loss of consciousness allegedly occurred; no history of mishandling could be elicited, but extensive diagnostic evaluations failed to yield any other explanation for the patient's conditions. We suspect that these infants were also victims of shaking, possibly intended to arouse them from an unresponsive state. 17 Failure to establish the history could simply reflect lack of awareness by the questioner or the caretaker of the significance of such an action, although denial ofhostile intention by an assailant is often encountered in such situations. 18 In three of our patients, retinal injury occurred in both eyes and was nearly symmetrical; in orie ofthese (case 2) a previous episode, probably involving similar trauma, had produced fundus hemorrhages but no apparent visual impairment. In one infant (case 5) there was bilateral involvement with substantially different outcomes in the two eyes, and in one (case 4) retinal damage occurred only in the left eye although initially hemorrhages were observed in the right eye as well. Observations concerning the initial occurrence in case 2 and the right eye in case 622
VOLUME 93 •
NUMBER 5
4 contrasted sharply at all stages with those made on the eyes that lost vision. All of the eyes that failed to recover (and none that did recover) showed impaired pupillary response to light from the time of initial evaluation through the final follow-up visit. In most the pupil was totally nonreactive. That this was due to an afferent rather than an efferent abnormality was demonstrated by the two asymmetrical cases, in which consensual movement of the pupil could be observed in the poorer eye. In the symmetrical cases the pupils were never noted to be widely dilated, and slow spontaneous constriction of the pupils was observed in at least one instance (case 1). Late retinal scarring was preceded by a striking migration of blood from the retina into the vitreous occurring several days to two weeks after injury in each of the three cases that was observed serially from the time of hospital admission. In one of the others (case 3) the vitreous was already blood-filled when the patient was first seen more than two weeks after injury, and the remaining child (case 5) did not have a fundus examination from the time of admission until five months later. Vitreous hemorrhages were dense, usually obscuring any view ofthe fundus, and resolved slowly over a period of several months to a year or more. In no case was organization of the vitreous or significant vitreoretinal traction documented. Blood was never observed in the vitreous of the eyes that retained good vision. Mushin noted that presence of vitreous hemorrhage in four of six abused infants who did not appear to have sustained direct blows to the eye but who ultimately showed retinal damage. 4 In two ofthese, blood was noted to have broken through into the vitreous from "subhyaloid" hemorrhages; in both cases the retina was damaged in the eye with vitreous involvement while the other eye recovered completely. Among eight infants in Mushin's series whose hemorrhages resolved without retinal scarring bilaterally, there were none in whom blood entered the vitreous. In our patients the acute appearance of the retina was generally similar in eyes that sustained permanent damage and those that did not: intraretinal and preretinal hemorrhages were noted in both. One dramatic feature was present only in cases that failed to recover, however. This was a large cystic or dome-like lesion in the macular region, completely or partially filled with blood. The fluid level formed by the blood in these cavities was similar to that which is characteristic of preretinal hemorrhages, but three independent observers described the lesions as appearing to be intraretinal cysts or retinoschisis. In case 1, in addition to a large macular cyst, there were a number of smaller similar lesions scattered in the posterior portion of the retina bilaterally. The left eye in case 4 had apparent schisis of the macula; the right eye, which recovered, had none. This appearance was not documented during the acute stage in the remaining cases (two of which were not examined by an ophthalmologist prior to the development of vitreous hemorrhage), but in all three of these patients macular abnormalities suggestive of retinoschisis could be seen after the vitreous cleared. A cystic lesion appar-
GREENWALD, et al •
ently filled with clear fluid occupied one of the maculas in each of cases 2 and 5, and in case 3 a whitish perimacular ring of retinal thickening, seeming to demarcate the base of a schisis cavity missing its inner wall, produced a crater-like lesion in one eye. Similar macular scars in the eyes of battered infants have been described previously.3.4 In cases 1 through 4 the peripheral retina appeared atrophic and gliotic and the retinal blood vessels were markedly narrowed in the chronic stage. Optic atrophy was obvious. The last patient (case 5), who retained 20/ 400 vision and a direct pupillary light reaction in his poorer eye, had fundus changes that suggested damage largely confined to the posterior pole, with temporal disc pallor only and vessels of nearly normal caliber. Interestingly, in this case alone there was a significant pigmentary disturbance in the macular region. Electroretinography (ERG) was clearly abnormal in all ofthe eyes that lost vision, showing absence or significant reduction of the positive B-wave with relatively good preservation of the negative A-wave. This finding was documented within a month of injury in one patient (case 2) and as late as six years afterwards in another (case 5). The right eye of case 4, which recovered completely, had a normal electroretinogram. Our electroretinographic data indicate that damage to the inner layers of the retina was primarily responsible for visual loss in our patients. It is unlikely that a rise in retinal venous pressure due either to hemodynamic factors or to increased intracranial pressure was the causative factor. Intraocular hemorrhages associated with intracranial hemorrhage or venous congestion in young persons do not as a rule produce retinal scarring unless organization of the vitreous leads to tractional detachment. 14- 16 Central retinal artery occlusion, possibly due to fat or air embolization from remote sites of injury, could explain the ERG abnormalities and the sclerotic appearance of the blood vessels in cases 1 through 3. It is difficult, however, to reconcile this mechanism with the presence of intraraetinal cavities in the macula, particularly in the patient (case 5) whose pathology appeared to be confined to the posterior pole. Ocular siderosis can produce a negative ERG 19 and may occur in consequence of severe vitreous hemorrhage. 20 None of our cases showed the characteristic progression of ERG changes that typically occurs in siderosis, however, and this condition also has no special predilection for the macula. We propose the following explanation to account for the features that characterize traumatic retinoschisis in battered babies: When an infant is shaken, its head is subjected to repetitive accelerations and decelerations as it whiplashes back and forth. A consequence is movement of the brain within the infant's relatively spacious cranium, which may disrupt bridging veins to cause the subdural hemorrhages so often seen in such patients. 12 Similar forces act on the eyes. One of their effects would be to make the relatively dense lens move forward and back within the ocular fluids. In infancy firm attachments exist between the lens, the vitreous gel, and the retina, especially the macular region. 21 ·22 Transmission of force through
TRAUMATIC RETINOSCHISIS
these connections could result momentarily in significant traction on the retina, particularly in the posterior pole. This abrupt tugging on the retina could create a separation along some plane within the tissue, possibly more than one. A very superficial splitting might disrupt only a few surface vessels, creating preretinal hemorrhage but leaving the retina functionally intact. Splitting external to the photoreceptors with disruption of the pigment epithelium and choriocapillaris might cause subretinal hemorrhage and late pigmentary disturbance. If schisis occurred anywhere between the nerve fiber layer and the outer nuclear layer, more serious consequences would be likely: breaking of the neural connections between the outer and inner layers of the retina, and rupture of capillaries from the retinal circulation extending into the inner retinal layers. Loss of function in the inner retina following shaking trauma could thus be due to direct tissue damage or to ischemia; in either case the ERG would have the appearance we detected. The resulting potential space within the retina might fill with blood from the disrupted vessels to produce the cyst-like leisons we observed in several of our patients. Incomplete schisis could produce the same functional deficits without gross separation oflayers, accounting for the gray appearance of the peripheral retina and the extensive deep intraretinal hemorrhages that we noted. Necrosis of the inner layer, occurring after some delay due to hemodynamic distrubances, could account for the late release of blood into the vitreous that seems characteristic of this syndrome. Confirmation of this or any hypothesis concerning the pathogenesis of traumatic retinoschisis in abused infants clearly requires pathological evidence. We have been unable to discover any published account of autopsy findings in a battered child from which conclusions relevant to the patients described in this report can be drawn. Since mortality unfortunately is not rare in this condition,2·5·10·12·13 we anticipate that clinicopathological correlation will be forthcoming. For the present, early recognition of the characteristic features of traumatic retinoschisis-impai red pupillary light reaction, delayed migration of blood into the vitreous, macular schisis, and loss of the ERG B-wave-may aid the clinician in identifying trauma, most likely shaking, as the cause of retinal damage in an infant who presents without a definite history or other physical signs of abuse. The poor visual prognosis in afflicted eyes should be considered in planning the acute and long-term care of these children.
REFERENCES 1. Gilkes MJ, Mann TP. Fundi of battered babies. Lancet 1967; 2: 468-9. 2. Friendly OS. Ocular manifestations of physical child abuse. Trans Am Acad Ophthamol Otolaryngol1971; 75:318-32. 3. Harcourt 8, Hopkins D. Ophthalmic manifestations of the battered· baby syndrome. Br Med J 1971; 3:398-401. 4. Mushin AS. Ocular damage in the battered-baby syndrome. Br Med J 1971; 3:402-4.
623
OPHTHALMOLOGY
•
MAY 1986
•
VOLUME 93
•
NUMBER 5
14. Walsh FB, Hoyt WF. Clinial Neuro-Ophthalmology, 3d ed. Baltimore: Williams & Wilkins, 1969; 1786-7. 15. Khan SG, Frenkel M. lntravitreal hemorrhage associated with rapid increase in intracranial pressure (Terson's syndrome). Am JOphthalmol 1975; 80:37-43. 16. von Barsewisch B. Perinatal Retinal Haemorrhages; Morphology, Aetiology and Significance. Berlin: Springer-Verlag, 1979.
5. Mushin A, Morgan G. Ocular injury in the battered baby syndrome; report of two cases. Br J Ophthalmol 1971; 55:343-7. 6. Jensen AD, Smith RE, Olson MI. Ocular clues to child abuse. J Pediatr Ophthalmol Strabismus 1971; 8:270-2. 7. Tomasi LG, Rosman NP. Purtscher retinopathy in the battered child syndrome. Am J Dis Child 1975; 129:1335-7. 8. Eisenbrey AB. Retinal hemorrhage in the battered child. Childs Brain 1979; 5:40-4. 9. Harley RD. Ocular manifestations of child abuse. J Pediatr Ophthalmol Strabismus 1980; 17:5-13. 10. Ober RR. Hemorrhagic retinopathy in infancy: a clinicopathologic report. J Pediatr Ophthalmol Strabismus 1980; 17:17-20. 11. San Martin R, Steinkuller PG, Nisbet RM. Retinopathy in the sexually abused battered child. Ann Ophthalmol1981; 13:89-91. 12. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremities with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396-403. 13. Ludwig S, Warman M. Shaken baby syndrome: a review of 20 cases. Ann Emerg Med 1984; 13:104-7.
17. Greenwald MJ. SBS and SIDS. Ann Emerg Med 1984; 13:1080. 18. Reece RM, Grodin MA. Recognition of nonaccidental injury. Pediatr Clin North Am 1985; 32(1):41-60. 19. Weinstein GW. Clinical visual electrophysiology. In: Duane TD, ed. Clinical Ophthalmology. Philadelphia: Harper & Row, 1985; Volume 3, Chapter 5. 20. Sugar HS, Kobernick SD, Weingarten JE. Hematogenous siderosis of local cause. Am J Ophthalmol1967; 64:749-56. 21. Duke-ElderS, Wybar KC. System of Ophthalmology. Vol. 2: The Anatomy of the Visual System. St. Louis: CV Mosby, 1961; 295-6. 22. Hogan MJ, Alvarado JA, Weddell JE. Histology of the Human Eye: An Atlas and Textbook. Philadelphia: WB Saunders, 1971; 613.
Discussion
by Andrea Cibis Tongue, MD The authors present five infants with clinical signs and symptoms of shaken baby syndrome described by Caffey. 1 All had CNS, retinal, and vitreous hemorrhages with a paucity of external signs of trauma. The authors noted that poor visual outcome was associated with afferent pupillary defects, vitreous hemorrhages, reduced or absent ERG B-wave, and large "cystic or dome-like lesions in the macular region, completely or partially filled with blood." Based on their clinical observations they hypothesize that these lesions are actually the result of retinoschisis and not simply sublaminar (preretinal) blood. The mechanism leading to retinoschisis is though by the authors to be one of vitreous traction on the retina during the time the baby is shaken. Schisis of the retina occurring between any layers may lead to interruption of neural connections and tearing of retinal capillaries or even the choriocapillaris, with resultant retinal, subretinal, and preretinal hemorrhages. Necrosis of the inner layer of the retina with escape of blood is postulated to give rise to the "late" vitreous hemorrhages. The authors' observation that the large and apparently elevated hemorrhages appear to be intraretinal and deep to the innermost retinal blood vessels is one that has not been emphasized previously. A review of fundus photos of patients with the shaken baby syndrome presented by me at the 1984 Academy Meeting indeed documented that retinal blood vessels could be seen to extend onto the surface of the large premacular hemorrhages in two patients. The photos also demonstrated the whitish or yellowwhite line described by the authors in the acute hemorrhagic phase and after the blood had completely resorbed. I therefore support the authors' impression that the large posterior pole hemorrhages in some cases are not simply preretinal or sublaminar but are deep to the large retinal vessels. However, it is unlikely that the basic lesion is one of retinoschisis rather than hemorrhage secondary to increased venous pressure. Hemorrhages in all layers of the retina occur in anumber of non traumatic disorders associated with changes in cerebrovascular dynamics such as central retinal vein occlusion, high altitude retinopathy, 2 and subarachnoid hemorrhage secondary to ruptured intracranial aneurysms. 3 Smith et a! produced pre-
624
retinal and retinal hemorrhages experimentally in a monkey by acutely raising intracranial pressure with saline infusion into the cisterna magna. 4 A separate subdural hemorrhage of the optic nerve sheath also occurred. They observed venous dilatation immediately on increase of the intracranial pressure, indicating acute cerebral and retinal circulatory changes, but observed the hemorrhage only after the third period of induced pressure rise. In infants the vascular system may be particularly susceptible to abrupt changes in pressure. The vessels may be more fragile than in adults, and the normally lower systemic blood pressure, higher cardiac rate, as well as rapid onset of metabolic acidosis with hypoxia, may affect the cerebrovascular hemodynamic forces more readily than in adults. Since cerebral anoxia and ischemia occur secondary to microvascular changes in experimental intracranial hypertension, certainly it is not unreasonable to postulate concomitant retinal anoxia and ischemia. 5 It may be the extent and location of the retinal ischemia that is the most critical factor in the production of visual loss, just as the extent and location of cerebral ischemia is the most critical factor in the resultant neurologic functional loss. Cortical atrophy and infarction, which can be massive in spite of relatively minor acute intracranial hemorrhages in these infants, may play a major role in the permanent visual deficit or may simply reflect the extent of cerebral and possible concomitant retinal anoxia. The authors' findings of absent or significantly reduced ERG B-wave potentials in eyes with poor visual outcome would support the concept of retinal ischemia involving the inner nuclear and plexiform layers. Sabates et al reported a disproportionately decreased B-wave in patients with venous stais retinopathy. 6 Interestingly in Sabates and co-workers' series ERG abnormalities could not be correlated with visual outcome. In that respect the authors' observation is of interest and hopefully will stimulate further investigation in this area. Nickel's and Hoyt's report of markedly depressed or absent ERG in babies who had sustained CNS hypoxia and severe visual impairment but with subsequent recovery of vision as well as the ERG raises the question of optimal timing of ERG testing in the shaken baby syndrome, particularly if respiratory arrest occurred. 7 Dr. Gerald Christensen presented a pathology specimen of
GREENWALD, et al
•
an eye obtained from a 51fz-month-old infant with typical clinical signs and symptoms of shaken baby syndrome at the Georgiana Dvorak Theobald Society in San Antonio, Texas in spring of 1985. Clinical examination before death by a pediatrician had revealed extensive retinal hemorrhages and "probable retinal detachments." On gross pathologic examination bilateral vitreous hemorrhages with liquefaction of the vitreous body, diffuse retinal hemorrhages, most dense in the posterior pole were noted. Microscopic examination demonstrated diffuse hemorrhage of the central as well as peripheral retina. The hemorrhage was most marked in the inner retinal layers, especially the nerve fiber layer and ganglion cell layer. Ganglion cell degeneration was most extensive within the macular area underlying the large sublaminar hemorrhage. Necrosis of cells of the inner nuclear layer as well as edema of the outer plexiform layer was noted. Some blood could be seen in the subretinal space, as well as along the vitreal surface of the inner limiting membrane. There was no evidence in any part of the specimen of retinoschisis or retinal detachment. The pathology of this eye therefore would not support the hypothesis of retinoschisis as outlined by the authors. The pathologic findings would also support the concept that vitreous hemorrhage simply occurs secondary to breakthrough of blood below the internal limiting membrane into the vitreous. This may be facilitated by the relatively thin internal limiting membrane found in the posterior pole of infant eyes. 8 The "late" occurrence of vitreous hemorrhage as observed by the authors is most likely secondary to the timing of vitreous liquefaction rather than necrosis of the retina. Vitreous hemorrhages were observed by me to be present in three children with shaken baby syndrome within one to two days of hospital admission. Initially the hemorrhages were small and globular in shape, but clearly intravitreal. In one case, diffuse vitreous opacification occurred one week later, and in the other two the blood simply appeared to spread out a little more in the posterior pole region but never completely blocked an ophthalmoscopic view of the fundus. Contrary to the findings of the authors, vitreous hemorrhage does not always imply a poor visual prognosis. Two of the cases I described at the American Academy of Ophthalmology in 1984 had extension of blood into the vitreous along with massive macular or posterior pole retinal hemorrhages. Both infants regained normal visual function. A third infant had unilateral retinal hemorrhages only, which cleared within 17 days. This child
TRAUMATIC RETINOSCHISIS
remains totally blind, probably secondary to severe cortical atrophy, which can be demonstrated on CT scan. Thus, vitreous hemorrhages and large sublaminar macular hemorrhages do not preclude a good visual prognosis, nor does absence of them guarantee a good visual outcome. In summary, I congratulate the authors on their astute clinical observations of the heretofore unpublished clinical findings in this disease. The observation of afferent pupillary and ERG Bwave abnormalities in eyes with poor visual outcome are intriguing and should be carefully examined by other investigators. Their hypothesis concerning the mechanisms of retinal damage and hemorrhage is interesting but not upheld by the pathologic specimen available to me. It appears unnecessary to invoke retinoschisis as the basis for the clinically observed retinal lesions. It is much more likely that the retinal hemorrhages are secondary to venous stasis, and that the retinal damage is secondary to retinal and cortical ischemia. References 1. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremeties with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396-403. 2. Shults WT, Swan KC. High altitude retinopathy in mountain climbers. Arch Ophthalmol 1975; 93:404-8. 3. Vanderlinden RG, Chisholm LD. Vitreous hemorrhages and sudden increased intracranial pressure. J Neurosurg 1974; 41:167-76. 4. Smith DC, Kearns TP, Sayre GP. Preretinal and optic nerve-sHeath hemorrhage: pathologic and experimental aspects in subarachnoid hemorrhage. Trans Am Acad Ophthalrnol Otolaryngol1957; 61:20111. 5. Shigeno T, Artigas J, Katoh G, et al. Cerebral edema following experimental subarachnoid hemorrhage. In: Cervos-Navarro J, Fritschka E, eds. Cerebral Microcirculation and Metabolism; International Erwin Riesch Symposium, Berlin, 1979. New York: Raven, 1981; 427-32. 6. Sabates R, Hirose T, McMeel JW. Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol 1983; 101:232-5. 7. Nickel BL, Hoyt CS. The hypoxic retinopathy syndrome. Am J Ophthalmol1982; 93:589-93. 8. Fine BS, Yanoff M. Ocular Histology; A Text and Atlas, 2nd ed. Hagerstown: Harper & Row, 1979; 97-99.
625
Abstract: Five infants who were victims of physical abuse had extensive bilateral retinal hemorrhages on initial evaluation and subsequently developed signs of permanent retinal damage. None showed external evidence of trauma to the eyes. Vitreous hemorrhage developed after a delay of several days or more in three cases that were followed closely from the time of the traumatic incident. In several eyes, apparent intraretinal blood-filled cavities were seen acutely in the macular region and elsewhere. Late scarring of the macula typically had a cystic or crater-like configuration. Electroretinography showed loss or reduction of the positive B-wave with preservation of the negative A-wave in every case. We propose that splitting of the retina resulting from the direct mechanical effects of violent shaking was responsible for all of these findings. [Key words: battered baby syndrome, child abuse, electroretinogram, macular lesion, retinal hemorrhage, retinoschisis, shaking trauma, subdural hemorrhage, vitreous hemorrhage.] Ophthalmology 93:618-625, 1986
Numerous reports have documented the frequent occurrence of hemorrhages in the ocular fundi of infants who have been physically abused. 1 ~ 11 Subretinal, retinal, preretinal, subhyaloid, and vitreous hemorrhages have been described. In most cases these are bilateral, and typically periocular and anterior segment signs of trauma are absent, suggesting an etiology other than direct contusion of the globe. Very commonly there is associated intracranial hemorrhage, often without skull fracture or external signs of a blow to the head. Caffey and others have argued convincingly that such cases may result from violent manual shaking by an adult, with repeated whiplashing of the infant's inadequately supported headY· 13 The pathogenesis of intraocular hemorrhages in battered babies remains uncertain. Retinal and vitreous hemorrhages are found frequently in patients with intracranial bleeding of any etiology, probably in consequence of acute elevation of intracranial pressure. 14•15 Their occurrence has been documented in abused infants with neither blood nor elevated pressure intracranially, From the Departments of Ophthalmology, Children's Hospital National Medical Center, Washington, DC, Northwestern University Medical School, Chicago. Presented at an Annual Meeting of the American Academy of Ophthalmology. Reprint requests to Mark J. Greenwald, MD, Division of Ophthalmology, Children's Memorial Hospital, 2300 Children's Plaza, Chicago, IL 60614.
618
however. 7 Hemodynamic stresses generated by chest compression or by extreme forms of abuse such as swinging the child around by its feet have been invoked in such cases. 1•7 In some abused infants with fundus hemorrhages, complete resolution occurs, while in others significant permanent visual loss is observed in one or both eyes. 3•4 Optic atrophy is typically present in such cases. Scarring and cyst formation in the macula have been reported. Afferent pupillary defects and strabismic deviation of unilaterally affected eyes may occur. The nature of the process that causes chronic disturbances in the retina and the optic nerve and the sequence through which these changes develop from acute hemorrhagic retinopathy have received little attention. Retinal hemorrhages occurring in infants in other circumstances (eg. in newborns following vaginal delivery) virtually always resolve to leave the fundus completely normal. 16 We report five cases of children in whom definite or probable physical abuse during infancy was associated with the development of extensive fundus hemorrhages, and in whom permanent scarring and decreased vision resulted. The evolution of physical findings was observed over a period of months to years and the functional status of the retina was assessed by means of electroretinography in every case. The consistent occurrence of certain distinctive features in these patients appears to define a clinical entity that we have designated "traumatic retinoschi-
GREENWALD, et al •
sis." The pathophysiological meachanism of this syndrome may be quite unlike those of other hemorrhagic retinopathies.
CASE REPORTS Case 1. A 9-month-old black girl was admitted to the intensive care unit (ICU) because of stupor, seizures, and episodic apnea. She had undergone surgery for congenital esotropia at age seven months; her ocular examination at that time had been otherwise normal and her general condition unremarkable. One week prior to hospitalization she developed an upper respiratory infection. On the day of admission, while in the care of a babysitter, she reportedly vomited, had a seizure, and became unresponsive. No history of physical abuse could be elicited. On arrival in the ICU the child was markedly obtunded and showed decerebrate posturing. The pupils were nonreactive and retinal hemorrhages were noted bilaterally. There was no external or radiographic evidence of trauma. On chest x-ray there was a right upper lobe infiltrate. Computed tomography did not disclose any intracranial hematoma. Lumbar puncture gave an opening pressure of 360 mm; in cerebrospinal fluid, glucose and protein were normal and there were 6500 red blood cells and 25 white blood cells (87% mononuclear) per cubic millimeter. All bacterial cultures and viral titers (herpes, cytomegalovirus, Epstein-Barr virus) were negative. Sickle hemoglobin was not present in red blood cells. Ophthalmological evaluation on the third hospital day confirmed that the pupils did not react to light, but they did vary spontaneously from 3 to 5 mm in diameter. There was no sign of visual interest and the eyes were tonically deviated downward. External and anterior segment structures were unremarkable and the vitreous was perfectly clear. On fundus examination, the discs appeared normal. Scattered throughout both fundi, but concentrated in the posterior poles, were a number of lesions that appeared to be intraretinal blood-filled cavities, within which the red blood cells had partially layered out inferiorly (Fig 1). The largest of these were in the macular regions bilaterally, extending out as far as the major vascular arcades. There was extensive hemorrhage without cyst formation elsewhere in the retina and the nonhemorrhagic retinal areas appeared thickened, opaque, and grayish in both eyes. On reexamination one week later there was possibly slight arousal in response to bright light, but no definite pupillary response could be documented. In contrast to the previous examination, the vitreous was filled with blood bilaterally and the fundi could not be seen at all. The child recovered consciousness but was left with severe spastic quadriparesis, seizures, and profound mental retardation. Subsequent computed tomography showed marked diffuse cerebral atrophy. Six months after discharge from the hospital, repeat ophthalmological evaluation demonstrated perststent lack of response to visual stimulation and nonreactivity ofthe pupils. There had been almost complete clearing of the vitreous in both eyes. The retinal vessels were markedly narrowed and sclerotic and there appeared to be extensive gliosis of the retina. An electroretinogram showed little or no positive B-wave with relatively good preservation of the negative A-wave (Fig 2). Reevaluation, including electroretinography, one year later was essentially unchanged. The consensus among medical personnel was that physical abuse was the cause of this child's devastating condition, but after investigation by governmental authorities the family and the child's babysitter were exonerated.
TRAUMATIC RETINOSCHISIS
Case 2. An 8-month-old black boy was hospitalized in a deeply stuporous state following a succession of generalized seizures. His foster mother admitted having shaken him in an attempt to stop the seizures. The child, who was in the care of a family that was attempting to adopt him, had suffered seizure-like episodes since four months of age, according to the foster parents. A similar episode had led to hospitalization at age five months. On that occasion the infant was alert and showed normal visual behavior at the time of admission. Both pupils were normally reactive. Ophthalmological evaluation revealed clear media and multiple retinal and preretinal hemorrhages in the posterior pole of both eyes, with a pale appearance of the surrounding retina resembling Berlin's edema. Computed tomography demonstrated a small subdural hematoma on the left side, from which 10 cc of blood was aspirated. There were no signs of soft tissue injury or fractures. Developmental progress was normal for that age, and the child appeared well nourished. An electroencephalogram done several weeks after discharge showed spikes in the left parietal region consistent with a focal convulsive disorder. The family was investigated because of suspicion of child abuse and received a favorable assessment. At the time of readmission to the hospital the infant was responsive only to deep pain and showed signs of left hemiplegia. Computed tomography demonstrated bilateral subdural hematomas. Ophthalmological evaluation showed no evidence of responsiveness to visual stimulation. The pupils were both 6 mm in diameter and nonreactive to light. The eyes were divergent with marked limitation of rotation in response to vestibular stimulation. External and anterior segment structures were essentially normal. In both fundi there were noted to be extensive intraretinal and subretinal helmorrhages with a small amount of preretinal hemorrhage. The nonhemorrhagic portions of the retina appeared grayish and opaque. The discs were normal in appearance and the vitreous was clear. Two weeks after admission, reexamination disclosed that the vitreous had become filled with blood in both eyes, with almost complete obscuration of the fundi. The pupils remained nonreactive. An electroretinogram recorded one week later (with the vitreous still densely hemorrhagic) showed almost complete extinction of the B-wave with relatively good preservation of the A-wave in the right eye and a very low voltage response that was difficult to interpret in the left eye. The child remained hospitalized for one month. He recovered consciousness but remained hemiparetic and subsequently showed moderately severe mental retardation. Bilateral subdural-peritoneal shunts were required to prevent reaccumulation of subdural fluid. Ophthalmological reevaluation one year later again demonstrated the absence of any detectable visual function. The pupils were still completely nonreactive. A large angle exotropia was present with bilateral limitation of adduction. The vitreous hemorrhage had cleared bilaterally. Fundus examination showed marked narrowing of the retinal vessels and pallor ofboth discs. In the right macula there was a large intraretinal cyst or schisis cavity surrounded by a ring of apparent gliosis. In the left eye there was no discrete macular lesion but extensive gliosis was present in the posterior pole and vessels appeared to extend into the vitreous from the disc. During the second hospitalization, x-rays had disclosed a fracture of the left tibia. Reassessment of the family situation led to the child's being placed in a different home, and to criminal prosecution and conviction of the original foster mother. Case 3. A 10-month-old black girl sustained severe head trauma when she was assaulted by her babysitter's boyfriend. Prior to this she had been in good health and was developing
619
RE LE
RE
LE
620
Fig I. Top left. case I, right eye. Artist's rendering of acute fundus appearance. Fig 2. Middle lefi, case I. Electroretinogram recorded six
months after onset of retinopathy. Full field white flash , intensity 16 X 10 3 ft-L, duration 10 microseconds. Cornea positivity represented by upward deflection. Calibration symbol (lower right corner) represents 20 milliseconds horizontally and 100 microvolts vertically. Fig 3. Bottom /e.fi, case 4. Electroretinogram (ERG) recorded 2 1/2 months after onset of retinopathy. Both eyes had extensive retinal hemorrhages, but only the left had an impaired pupillary light response, delayed appearance of blood in the vitreous, and macular schisis. ERG parameters are the same as in Figure 2. Fig 4. Top right, case 5, right eye. Fundus appearance three years after onset of retinopathy. Fig 5. Bottom right. case 5, right eye. Electroretinogram recorded six years after onset of retinopathy. Parameters are the same as in Figure 2.
GREENWALD, et al •
normally. On arrival in the emergency room she was stuporous, responding only to pain. Both pupils were poorly reactive. Skull x-rays and computed tomography revealed a right occipital fracture and a large left subdural hemorrhage. The intracranial hematoma was evacuated acutely; it reaccumulated and a craniectomy with placement of drains was performed on the third day of hospitalization. Repeat computed tomography revealed a possible infarction of the brain in the distribution of the left posterior cerebral artery. One week after admission it was noted that the fundi could not be seen. Ophthalmological evaluation was performed on the 17th hospital day. There was a questionable blink response to bright light but both pupils were nonreactive at 5 mm diameter. External and anterior segment structures were unremarkable. Dense vitreous hemorrhage was present in both eyes; fundus details could barely be discerned. The child was discharged after nearly one month in the hospital alert and without focal neurologic deficits except for apparent blindness. Three months after injury there was still no definite evidence of any visual function and the pupils remained unresponsive to light. Only partial clearing of the vitreous hemorrhage had occurred; the fundi could still not be seen clearly, but B-scan ultrasonography demonstrated attached retinas. Electroretinography showed markedly diminished responses consisting only of initial negative potentials in both eyes. One year later, constant slow, roving, conjugate eye movements were noted. The right pupil was minimally reactive to direct light stimulation and the left pupil was completely nonreactive, showing a relative afferent defect. Vitreous hemorrhage had cleared entirely on the right and partially on the left to permit visualization of both fundi. The discs were pale and the vessels were markedly attenuated. Both retinas had a gliotic appearance, which was especially marked in a ring-shaped distribution surrounding the right macula, producing a crater-like appearance. The electroretinogram was repeated and showed essentially the same response noted previously. The child was last seen at age 4 years. Her intelligence was good. Profound visual impairment persisted, but light perception could be documented. Clearing of the vitreous hemorrhage was complete bilaterally. The appearance of the fundi was unchanged. Case 4. A 5-month-old white girl was hospitalized for seizures and obtundation. Her previous health and development had been normal. On the day of admission she had been irritable and sleepy. Late in the afternoon, while attended by a babysitter, she reportedly became rigid and unresponsive. No history of trauma or rough handling was obtained. The child was brought to the emergency room where tonic-clonic movements were observed. On admission she was lethargic and showed right hemiparesis with frequent brief episodes of right-sided jerking movements. The right pupil was normally reactive and the left was nonreactive. Retinal hemorrhages were noted bilaterally. Computed tomography showed a left subdural hemorrhage with a midline shift. There was no evidence of soft tissue injury or fractures. Ophthalmological consultation was obtained on the day after admission. Visual responsiveness could not be demonstrated. Vestibulo-ocular movements were intact. The right pupil reacted normally; the left showed no direct reaction but a normal consensual response (amaurotic pupil). External and anterior segment structures were normal and the vitreous was clear bilaterally. Multiple retinal and preretinal hemorrhages were present throughout the fundi, but concentrated in the posterior pole, and the nonhemorrhagic retina appeared edematous in both eyes. These abnormalities were more marked in the left eye. In addition, in the left eye only, a large dome-like elevation of the retinal surface in the posterior pole was observed, occupying most of the region within the temporal vascular arcades. The
TRAUMATIC RETINOSCHISIS
retina immediately surrounding this structure, which was described as retinoschisis, appeared thick and opague. On the tenth hospital day repeat eye examination showed no change in the pupils, with a persistent left afferent pupillary defect. In the right eye, the retinal hemorrhages had become smaller, the surrounding retina had recovered a nearly normal appearance, and the vitreous remained clear. On the left the vitreous had become filled with blood, which totally obscured the fundus. During two weeks of hospitalization the child was treated medically for cerebral edema and seizures but did not require surgery for her subdural hemorrhage, which resolved spontaneously. At discharge she was alert but had a mild persistent right hemiparesis. Reaccumulation of subdural fluid necessitated readmission for subdural-peritoneal shunt placement six weeks later. At that time ophthalmological evaluation showed normal fixation with the right eye and no fixation with the left. The pupils were unchanged from the first examination. The right fundus had recovered a completely normal appearance, while the left was still obscured by dense vitreous hemorrhage. B-scan ultrasonography demonstrated an attached retina in the left eye. The electroretinogram was normal on the right and on the left consisted only of the negative A-wave (Fig 3). The patient was last seen four months after the first hospitalization. Ocular findings were unchanged except for partial clearing of vitreous blood from the left eye. Although trauma was believed to be responsible for this child's condition, investigation of the case by governmental authorities did not lead to any action against the family. Case 5. A 2-month-old black boy was admitted to the hospital after being resuscitated by his father from an episode of apnea. The resuscitation measures had included shaking the baby as well as mouth to mouth ventilation, which was continued for an estimated ten minutes before spontaneous respiration returned. Prior to this the infant had been healthy except for the occurrence of a similar apneic spell two weeks earlier. In the emergency room he was noted to be alert and without focal neurological deficits. The right pupillary light reaction was impaired in comparison with the left. Retinal hemorrhages were observed bilaterally. Computed tomography demonstrated bilateral subdural hemorrhages. There were no other signs of trauma. The occurrence of apneic spells was documented during the period of hospitalization. After repeated reaccumulation of subdural fluid following aspiration, subdural-peritoneal shunts were placed bilaterally. The patient was discharged after three weeks. Ophthalmological consultation was not obtained during this hospitalization. The child was first seen in the eye clinic at age 7 months for evaluation of right esotropia, which had been noted by the family shortly after discharge from the hospital. Examination revealed poor fixation with the right eye and central steady maintained fixation with the left eye. Both pupils were reactive to light but an afferent defect was present on the right. Variable esotropia of moderate angle was present. External and anterior segment • structures were normal. There were fundus abnormalities bilaterally. On the right, the disc showed definite pallor, especially temporally. A large, elevated, apparently cystic lesion occupied the macula and the papillomacular area, surrounded by gliotic appearing retina. There was marked irregularity ofthe underlying retinal pigment epithelium. The disc appeared normal on the left but there was an unusual light reflection from the vitreoretinal interface and a mild disturbance of the retinal pigment epithelium. The retinal vessels were normal or slightly narrowed bilaterally. The child was followed for several years. His development progressed normally. Visual acuity at the last clinic visit was 20/ 400 in the right eye and 20/40 in the left. Findings on exami-
621
OPHTHALMOLOGY •
MAY 1986 •
nation remained approximately the same, except for some flattening of the cystic lesion in the right posterior pole (Fig 4). Strabismus correction was performed at age 3 years. An electroretinogram of acceptable quality was recorded six years after the traumatic episode. It showed reduction of the B-wave with an intact A-wave in both eyes (Fig 5). The hospital's child protection team investigated this case during the acute stage and concluded that the patient's injuries had resulted from unintentionally violent resuscitation measures performed by the father. No legal action was taken.
DISCUSSION All of the patients in our series came to medical attention during infancy, with ages ranging from 2 to 10 months. Three were girls and two were boys. Four of the five were black; the fifth was white. This racial distribution probably reflects the composition of the population that utilizes the hospital's emergency room. Subdural hemorrhages were present in four of our five cases, bilaterally in two. One of these children suffered major permanent brain damage; the other three recovered with only minor deficits aside from impaired vision. In the remaining case no intracranial hematoma was documented, but increased intracranial pressure was demonstrated acutely, and cerebral atrophy with severe neurological impairment developed subsequently. A skull fracture was present in only one patient, who was known to have been beaten. A fracture of the tibia was disclosed by a radiographic bone survey in another, who was believed to have been violently shaken. Clinical and laboratory evaluation failed to reveal any evidence of trauma other than ocular and central nervous system findings in the remaining three cases. A history of deliberate physical abuse was obtained in only one case. In two others a parent admitted having shaken the infant while trying to resuscitate it following loss of consciousness associated with a seizure or an apneic episode. In the remaining two cases the child was in the care of a babysitter when spontaneous loss of consciousness allegedly occurred; no history of mishandling could be elicited, but extensive diagnostic evaluations failed to yield any other explanation for the patient's conditions. We suspect that these infants were also victims of shaking, possibly intended to arouse them from an unresponsive state. 17 Failure to establish the history could simply reflect lack of awareness by the questioner or the caretaker of the significance of such an action, although denial ofhostile intention by an assailant is often encountered in such situations. 18 In three of our patients, retinal injury occurred in both eyes and was nearly symmetrical; in orie ofthese (case 2) a previous episode, probably involving similar trauma, had produced fundus hemorrhages but no apparent visual impairment. In one infant (case 5) there was bilateral involvement with substantially different outcomes in the two eyes, and in one (case 4) retinal damage occurred only in the left eye although initially hemorrhages were observed in the right eye as well. Observations concerning the initial occurrence in case 2 and the right eye in case 622
VOLUME 93 •
NUMBER 5
4 contrasted sharply at all stages with those made on the eyes that lost vision. All of the eyes that failed to recover (and none that did recover) showed impaired pupillary response to light from the time of initial evaluation through the final follow-up visit. In most the pupil was totally nonreactive. That this was due to an afferent rather than an efferent abnormality was demonstrated by the two asymmetrical cases, in which consensual movement of the pupil could be observed in the poorer eye. In the symmetrical cases the pupils were never noted to be widely dilated, and slow spontaneous constriction of the pupils was observed in at least one instance (case 1). Late retinal scarring was preceded by a striking migration of blood from the retina into the vitreous occurring several days to two weeks after injury in each of the three cases that was observed serially from the time of hospital admission. In one of the others (case 3) the vitreous was already blood-filled when the patient was first seen more than two weeks after injury, and the remaining child (case 5) did not have a fundus examination from the time of admission until five months later. Vitreous hemorrhages were dense, usually obscuring any view ofthe fundus, and resolved slowly over a period of several months to a year or more. In no case was organization of the vitreous or significant vitreoretinal traction documented. Blood was never observed in the vitreous of the eyes that retained good vision. Mushin noted that presence of vitreous hemorrhage in four of six abused infants who did not appear to have sustained direct blows to the eye but who ultimately showed retinal damage. 4 In two ofthese, blood was noted to have broken through into the vitreous from "subhyaloid" hemorrhages; in both cases the retina was damaged in the eye with vitreous involvement while the other eye recovered completely. Among eight infants in Mushin's series whose hemorrhages resolved without retinal scarring bilaterally, there were none in whom blood entered the vitreous. In our patients the acute appearance of the retina was generally similar in eyes that sustained permanent damage and those that did not: intraretinal and preretinal hemorrhages were noted in both. One dramatic feature was present only in cases that failed to recover, however. This was a large cystic or dome-like lesion in the macular region, completely or partially filled with blood. The fluid level formed by the blood in these cavities was similar to that which is characteristic of preretinal hemorrhages, but three independent observers described the lesions as appearing to be intraretinal cysts or retinoschisis. In case 1, in addition to a large macular cyst, there were a number of smaller similar lesions scattered in the posterior portion of the retina bilaterally. The left eye in case 4 had apparent schisis of the macula; the right eye, which recovered, had none. This appearance was not documented during the acute stage in the remaining cases (two of which were not examined by an ophthalmologist prior to the development of vitreous hemorrhage), but in all three of these patients macular abnormalities suggestive of retinoschisis could be seen after the vitreous cleared. A cystic lesion appar-
GREENWALD, et al •
ently filled with clear fluid occupied one of the maculas in each of cases 2 and 5, and in case 3 a whitish perimacular ring of retinal thickening, seeming to demarcate the base of a schisis cavity missing its inner wall, produced a crater-like lesion in one eye. Similar macular scars in the eyes of battered infants have been described previously.3.4 In cases 1 through 4 the peripheral retina appeared atrophic and gliotic and the retinal blood vessels were markedly narrowed in the chronic stage. Optic atrophy was obvious. The last patient (case 5), who retained 20/ 400 vision and a direct pupillary light reaction in his poorer eye, had fundus changes that suggested damage largely confined to the posterior pole, with temporal disc pallor only and vessels of nearly normal caliber. Interestingly, in this case alone there was a significant pigmentary disturbance in the macular region. Electroretinography (ERG) was clearly abnormal in all ofthe eyes that lost vision, showing absence or significant reduction of the positive B-wave with relatively good preservation of the negative A-wave. This finding was documented within a month of injury in one patient (case 2) and as late as six years afterwards in another (case 5). The right eye of case 4, which recovered completely, had a normal electroretinogram. Our electroretinographic data indicate that damage to the inner layers of the retina was primarily responsible for visual loss in our patients. It is unlikely that a rise in retinal venous pressure due either to hemodynamic factors or to increased intracranial pressure was the causative factor. Intraocular hemorrhages associated with intracranial hemorrhage or venous congestion in young persons do not as a rule produce retinal scarring unless organization of the vitreous leads to tractional detachment. 14- 16 Central retinal artery occlusion, possibly due to fat or air embolization from remote sites of injury, could explain the ERG abnormalities and the sclerotic appearance of the blood vessels in cases 1 through 3. It is difficult, however, to reconcile this mechanism with the presence of intraraetinal cavities in the macula, particularly in the patient (case 5) whose pathology appeared to be confined to the posterior pole. Ocular siderosis can produce a negative ERG 19 and may occur in consequence of severe vitreous hemorrhage. 20 None of our cases showed the characteristic progression of ERG changes that typically occurs in siderosis, however, and this condition also has no special predilection for the macula. We propose the following explanation to account for the features that characterize traumatic retinoschisis in battered babies: When an infant is shaken, its head is subjected to repetitive accelerations and decelerations as it whiplashes back and forth. A consequence is movement of the brain within the infant's relatively spacious cranium, which may disrupt bridging veins to cause the subdural hemorrhages so often seen in such patients. 12 Similar forces act on the eyes. One of their effects would be to make the relatively dense lens move forward and back within the ocular fluids. In infancy firm attachments exist between the lens, the vitreous gel, and the retina, especially the macular region. 21 ·22 Transmission of force through
TRAUMATIC RETINOSCHISIS
these connections could result momentarily in significant traction on the retina, particularly in the posterior pole. This abrupt tugging on the retina could create a separation along some plane within the tissue, possibly more than one. A very superficial splitting might disrupt only a few surface vessels, creating preretinal hemorrhage but leaving the retina functionally intact. Splitting external to the photoreceptors with disruption of the pigment epithelium and choriocapillaris might cause subretinal hemorrhage and late pigmentary disturbance. If schisis occurred anywhere between the nerve fiber layer and the outer nuclear layer, more serious consequences would be likely: breaking of the neural connections between the outer and inner layers of the retina, and rupture of capillaries from the retinal circulation extending into the inner retinal layers. Loss of function in the inner retina following shaking trauma could thus be due to direct tissue damage or to ischemia; in either case the ERG would have the appearance we detected. The resulting potential space within the retina might fill with blood from the disrupted vessels to produce the cyst-like leisons we observed in several of our patients. Incomplete schisis could produce the same functional deficits without gross separation oflayers, accounting for the gray appearance of the peripheral retina and the extensive deep intraretinal hemorrhages that we noted. Necrosis of the inner layer, occurring after some delay due to hemodynamic distrubances, could account for the late release of blood into the vitreous that seems characteristic of this syndrome. Confirmation of this or any hypothesis concerning the pathogenesis of traumatic retinoschisis in abused infants clearly requires pathological evidence. We have been unable to discover any published account of autopsy findings in a battered child from which conclusions relevant to the patients described in this report can be drawn. Since mortality unfortunately is not rare in this condition,2·5·10·12·13 we anticipate that clinicopathological correlation will be forthcoming. For the present, early recognition of the characteristic features of traumatic retinoschisis-impai red pupillary light reaction, delayed migration of blood into the vitreous, macular schisis, and loss of the ERG B-wave-may aid the clinician in identifying trauma, most likely shaking, as the cause of retinal damage in an infant who presents without a definite history or other physical signs of abuse. The poor visual prognosis in afflicted eyes should be considered in planning the acute and long-term care of these children.
REFERENCES 1. Gilkes MJ, Mann TP. Fundi of battered babies. Lancet 1967; 2: 468-9. 2. Friendly OS. Ocular manifestations of physical child abuse. Trans Am Acad Ophthamol Otolaryngol1971; 75:318-32. 3. Harcourt 8, Hopkins D. Ophthalmic manifestations of the battered· baby syndrome. Br Med J 1971; 3:398-401. 4. Mushin AS. Ocular damage in the battered-baby syndrome. Br Med J 1971; 3:402-4.
623
OPHTHALMOLOGY
•
MAY 1986
•
VOLUME 93
•
NUMBER 5
14. Walsh FB, Hoyt WF. Clinial Neuro-Ophthalmology, 3d ed. Baltimore: Williams & Wilkins, 1969; 1786-7. 15. Khan SG, Frenkel M. lntravitreal hemorrhage associated with rapid increase in intracranial pressure (Terson's syndrome). Am JOphthalmol 1975; 80:37-43. 16. von Barsewisch B. Perinatal Retinal Haemorrhages; Morphology, Aetiology and Significance. Berlin: Springer-Verlag, 1979.
5. Mushin A, Morgan G. Ocular injury in the battered baby syndrome; report of two cases. Br J Ophthalmol 1971; 55:343-7. 6. Jensen AD, Smith RE, Olson MI. Ocular clues to child abuse. J Pediatr Ophthalmol Strabismus 1971; 8:270-2. 7. Tomasi LG, Rosman NP. Purtscher retinopathy in the battered child syndrome. Am J Dis Child 1975; 129:1335-7. 8. Eisenbrey AB. Retinal hemorrhage in the battered child. Childs Brain 1979; 5:40-4. 9. Harley RD. Ocular manifestations of child abuse. J Pediatr Ophthalmol Strabismus 1980; 17:5-13. 10. Ober RR. Hemorrhagic retinopathy in infancy: a clinicopathologic report. J Pediatr Ophthalmol Strabismus 1980; 17:17-20. 11. San Martin R, Steinkuller PG, Nisbet RM. Retinopathy in the sexually abused battered child. Ann Ophthalmol1981; 13:89-91. 12. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremities with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396-403. 13. Ludwig S, Warman M. Shaken baby syndrome: a review of 20 cases. Ann Emerg Med 1984; 13:104-7.
17. Greenwald MJ. SBS and SIDS. Ann Emerg Med 1984; 13:1080. 18. Reece RM, Grodin MA. Recognition of nonaccidental injury. Pediatr Clin North Am 1985; 32(1):41-60. 19. Weinstein GW. Clinical visual electrophysiology. In: Duane TD, ed. Clinical Ophthalmology. Philadelphia: Harper & Row, 1985; Volume 3, Chapter 5. 20. Sugar HS, Kobernick SD, Weingarten JE. Hematogenous siderosis of local cause. Am J Ophthalmol1967; 64:749-56. 21. Duke-ElderS, Wybar KC. System of Ophthalmology. Vol. 2: The Anatomy of the Visual System. St. Louis: CV Mosby, 1961; 295-6. 22. Hogan MJ, Alvarado JA, Weddell JE. Histology of the Human Eye: An Atlas and Textbook. Philadelphia: WB Saunders, 1971; 613.
Discussion
by Andrea Cibis Tongue, MD The authors present five infants with clinical signs and symptoms of shaken baby syndrome described by Caffey. 1 All had CNS, retinal, and vitreous hemorrhages with a paucity of external signs of trauma. The authors noted that poor visual outcome was associated with afferent pupillary defects, vitreous hemorrhages, reduced or absent ERG B-wave, and large "cystic or dome-like lesions in the macular region, completely or partially filled with blood." Based on their clinical observations they hypothesize that these lesions are actually the result of retinoschisis and not simply sublaminar (preretinal) blood. The mechanism leading to retinoschisis is though by the authors to be one of vitreous traction on the retina during the time the baby is shaken. Schisis of the retina occurring between any layers may lead to interruption of neural connections and tearing of retinal capillaries or even the choriocapillaris, with resultant retinal, subretinal, and preretinal hemorrhages. Necrosis of the inner layer of the retina with escape of blood is postulated to give rise to the "late" vitreous hemorrhages. The authors' observation that the large and apparently elevated hemorrhages appear to be intraretinal and deep to the innermost retinal blood vessels is one that has not been emphasized previously. A review of fundus photos of patients with the shaken baby syndrome presented by me at the 1984 Academy Meeting indeed documented that retinal blood vessels could be seen to extend onto the surface of the large premacular hemorrhages in two patients. The photos also demonstrated the whitish or yellowwhite line described by the authors in the acute hemorrhagic phase and after the blood had completely resorbed. I therefore support the authors' impression that the large posterior pole hemorrhages in some cases are not simply preretinal or sublaminar but are deep to the large retinal vessels. However, it is unlikely that the basic lesion is one of retinoschisis rather than hemorrhage secondary to increased venous pressure. Hemorrhages in all layers of the retina occur in anumber of non traumatic disorders associated with changes in cerebrovascular dynamics such as central retinal vein occlusion, high altitude retinopathy, 2 and subarachnoid hemorrhage secondary to ruptured intracranial aneurysms. 3 Smith et a! produced pre-
624
retinal and retinal hemorrhages experimentally in a monkey by acutely raising intracranial pressure with saline infusion into the cisterna magna. 4 A separate subdural hemorrhage of the optic nerve sheath also occurred. They observed venous dilatation immediately on increase of the intracranial pressure, indicating acute cerebral and retinal circulatory changes, but observed the hemorrhage only after the third period of induced pressure rise. In infants the vascular system may be particularly susceptible to abrupt changes in pressure. The vessels may be more fragile than in adults, and the normally lower systemic blood pressure, higher cardiac rate, as well as rapid onset of metabolic acidosis with hypoxia, may affect the cerebrovascular hemodynamic forces more readily than in adults. Since cerebral anoxia and ischemia occur secondary to microvascular changes in experimental intracranial hypertension, certainly it is not unreasonable to postulate concomitant retinal anoxia and ischemia. 5 It may be the extent and location of the retinal ischemia that is the most critical factor in the production of visual loss, just as the extent and location of cerebral ischemia is the most critical factor in the resultant neurologic functional loss. Cortical atrophy and infarction, which can be massive in spite of relatively minor acute intracranial hemorrhages in these infants, may play a major role in the permanent visual deficit or may simply reflect the extent of cerebral and possible concomitant retinal anoxia. The authors' findings of absent or significantly reduced ERG B-wave potentials in eyes with poor visual outcome would support the concept of retinal ischemia involving the inner nuclear and plexiform layers. Sabates et al reported a disproportionately decreased B-wave in patients with venous stais retinopathy. 6 Interestingly in Sabates and co-workers' series ERG abnormalities could not be correlated with visual outcome. In that respect the authors' observation is of interest and hopefully will stimulate further investigation in this area. Nickel's and Hoyt's report of markedly depressed or absent ERG in babies who had sustained CNS hypoxia and severe visual impairment but with subsequent recovery of vision as well as the ERG raises the question of optimal timing of ERG testing in the shaken baby syndrome, particularly if respiratory arrest occurred. 7 Dr. Gerald Christensen presented a pathology specimen of
GREENWALD, et al
•
an eye obtained from a 51fz-month-old infant with typical clinical signs and symptoms of shaken baby syndrome at the Georgiana Dvorak Theobald Society in San Antonio, Texas in spring of 1985. Clinical examination before death by a pediatrician had revealed extensive retinal hemorrhages and "probable retinal detachments." On gross pathologic examination bilateral vitreous hemorrhages with liquefaction of the vitreous body, diffuse retinal hemorrhages, most dense in the posterior pole were noted. Microscopic examination demonstrated diffuse hemorrhage of the central as well as peripheral retina. The hemorrhage was most marked in the inner retinal layers, especially the nerve fiber layer and ganglion cell layer. Ganglion cell degeneration was most extensive within the macular area underlying the large sublaminar hemorrhage. Necrosis of cells of the inner nuclear layer as well as edema of the outer plexiform layer was noted. Some blood could be seen in the subretinal space, as well as along the vitreal surface of the inner limiting membrane. There was no evidence in any part of the specimen of retinoschisis or retinal detachment. The pathology of this eye therefore would not support the hypothesis of retinoschisis as outlined by the authors. The pathologic findings would also support the concept that vitreous hemorrhage simply occurs secondary to breakthrough of blood below the internal limiting membrane into the vitreous. This may be facilitated by the relatively thin internal limiting membrane found in the posterior pole of infant eyes. 8 The "late" occurrence of vitreous hemorrhage as observed by the authors is most likely secondary to the timing of vitreous liquefaction rather than necrosis of the retina. Vitreous hemorrhages were observed by me to be present in three children with shaken baby syndrome within one to two days of hospital admission. Initially the hemorrhages were small and globular in shape, but clearly intravitreal. In one case, diffuse vitreous opacification occurred one week later, and in the other two the blood simply appeared to spread out a little more in the posterior pole region but never completely blocked an ophthalmoscopic view of the fundus. Contrary to the findings of the authors, vitreous hemorrhage does not always imply a poor visual prognosis. Two of the cases I described at the American Academy of Ophthalmology in 1984 had extension of blood into the vitreous along with massive macular or posterior pole retinal hemorrhages. Both infants regained normal visual function. A third infant had unilateral retinal hemorrhages only, which cleared within 17 days. This child
TRAUMATIC RETINOSCHISIS
remains totally blind, probably secondary to severe cortical atrophy, which can be demonstrated on CT scan. Thus, vitreous hemorrhages and large sublaminar macular hemorrhages do not preclude a good visual prognosis, nor does absence of them guarantee a good visual outcome. In summary, I congratulate the authors on their astute clinical observations of the heretofore unpublished clinical findings in this disease. The observation of afferent pupillary and ERG Bwave abnormalities in eyes with poor visual outcome are intriguing and should be carefully examined by other investigators. Their hypothesis concerning the mechanisms of retinal damage and hemorrhage is interesting but not upheld by the pathologic specimen available to me. It appears unnecessary to invoke retinoschisis as the basis for the clinically observed retinal lesions. It is much more likely that the retinal hemorrhages are secondary to venous stasis, and that the retinal damage is secondary to retinal and cortical ischemia. References 1. Caffey J. The whiplash shaken infant syndrome: manual shaking by the extremeties with whiplash-induced intracranial and intraocular bleedings, linked with residual permanent brain damage and mental retardation. Pediatrics 1974; 54:396-403. 2. Shults WT, Swan KC. High altitude retinopathy in mountain climbers. Arch Ophthalmol 1975; 93:404-8. 3. Vanderlinden RG, Chisholm LD. Vitreous hemorrhages and sudden increased intracranial pressure. J Neurosurg 1974; 41:167-76. 4. Smith DC, Kearns TP, Sayre GP. Preretinal and optic nerve-sHeath hemorrhage: pathologic and experimental aspects in subarachnoid hemorrhage. Trans Am Acad Ophthalrnol Otolaryngol1957; 61:20111. 5. Shigeno T, Artigas J, Katoh G, et al. Cerebral edema following experimental subarachnoid hemorrhage. In: Cervos-Navarro J, Fritschka E, eds. Cerebral Microcirculation and Metabolism; International Erwin Riesch Symposium, Berlin, 1979. New York: Raven, 1981; 427-32. 6. Sabates R, Hirose T, McMeel JW. Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol 1983; 101:232-5. 7. Nickel BL, Hoyt CS. The hypoxic retinopathy syndrome. Am J Ophthalmol1982; 93:589-93. 8. Fine BS, Yanoff M. Ocular Histology; A Text and Atlas, 2nd ed. Hagerstown: Harper & Row, 1979; 97-99.
625