From Manchester Royal Eye Hospital, Manchester, United Kingdom.
The authors have no financial or proprietary interest in the materials presented herein.
Address correspondence to Vinod Sharma, MRCOphth, Manchester Royal Eye Hospital, Oxford Road, Manchester M13 9WH, United Kingdom. E-mail: email@example.com
The hyaloid artery is the termination of the fetal ophthalmic artery and extends from the optic nerve to the posterior surface of the lens, where it terminates by arborization. It starts to regress as its branches become occluded by macrophages, and this process is usually complete near term.
Persistence of the hyaloid artery or some part of it is a common congenital anomaly during the neonatal period. It is seen mostly as persistent parts of the artery at the disc, which is called a Bergmeister’s papilla, or at the posterior lens capsule, which is called Mittendorf’s dot. Persistence of the entire artery is less common. The persistent hyaloid artery is usually in the form of a thin cord and active blood flow in the hyaloid artery during the postpartum period is rare,1 so reports of hemorrhage from a hyaloid artery are rare.2 It is observed in 3% of infants born at term and in up to 90% of premature infants. Its involution is complete in a few weeks during the postpartum period.3
Terson syndrome is defined as any intraocular hemorrhage in association with intracranial hemorrhage and raised intracranial pressure. The classic presentation is with subhyaloid hemorrhage. It is a rare finding in children,4 and there have been no reports in the literature as a finding in premature infants.
A premature male infant, born at 28 + 4 weeks gestation and weighing 1,250 grams underwent routine retinopathy of prematurity (ROP) screening at 32 weeks corrected gestational age. The infant had not left the neonatal intensive care unit since birth. Systemically, among other problems, the infant was floppy. Cranial ultrasound revealed a grade 4 intraventricular hemorrhage with raised intracranial pressure later, causing hydrocephalus with increasing head circumference.
On fundus examination, the infant had a resolving vitreous hemorrhage leading to a whitish opacity in front of the posterior pole in the right eye (Fig. 1). The peripheral retina was visible and revealed stage I, zone 2 ROP. The left eye revealed a patent but regressing hyaloid artery arising from the disc and extending to the mid vitreous (Fig. 2). There was stage I zone 2 ROP in the periphery (Fig. 3).
Figure 1. Fundus photograph of the right eye showing a dense opacity from resolving vitreous hemorrhage.
Figure 2. Fundus photograph of the left eye showing hyaloid vasculature (arrow).
Figure 3. Fundus photograph of the left eye showing stage 1, zone II retinopathy of prematurity.
The vitreous hemorrhage in the right eye had formed a dense ochre membrane obscuring the disc and macula. The infant was examined weekly until 39 weeks corrected gestational age. The dense ochre membrane persisted, showing no sign of resolution. It was decided to seek a vitreoretinal consultation due to the likelihood of visual deprivation caused by the central opacity.
At 39 weeks gestational age, the infant underwent a three-port vitrectomy using 23-gauge instruments. The scleral ports were made guided by transillumination. A lens-sparing core vitrectomy was performed to clear the visual axis and at the end of the procedure the scleral wounds were sutured with 6-0 polyglactin 910. Postoperatively, the infant started receiving topical prednisolone 1% four times a day, chloramphenicol 0.5% four times a day, and cyclopentolate 0.5% twice a day for 4 weeks.
A week later, the infant was making a good recovery with clear media, but owing to suspected meningitis was admitted in a peripheral hospital and was next seen 2 months postoperatively. On examination, the infant demonstrated poor fixation and visual behavior. Ocular media were clear in the right eye and fundus examination showed regressed ROP in both eyes but bilateral optic atrophy. A cycloplegic refraction revealed −11 diopters of myopia in the right eye and +1.5 diopters of hypermetropia in the left eye.
Bleeding from a persistent hyaloid artery is rare and can occur following rapid eye movements during sleep, trauma, and posterior vitreous detachment and can also occur spontaneously.
A persistent hyaloid artery has been associated with amblyopia, nystagmus, strabismus,2 and, uncommonly, vitreous hemorrhage. A significant hemorrhage can temporarily reduce the visual acuity. Older children and adults can be monitored while waiting for the vitreous hemorrhage to resolve, but a vitreous hemorrhage occurring in the neonatal period may lead to vision deprivation and can affect the development of fixation and lead to dense amblyopia if persistent beyond the critical period for visual development.
Terson syndrome is defined as intraocular hemorrhage in association with intracranial hemorrhage and raised intracranial pressure. Prospective studies in adults suggest an incidence of 17% to 45%.5 Schloff et al. reported the incidence of Terson syndrome to be less than 8% in children.4
The pathophysiology of Terson syndrome is controversial. There is an increase in pressure within the retinal vasculature leading to rupture of the capillaries and venules, which results in intraretinal or preretinal bleeding. Some believe this is caused by the increase in intracranial pressure being transmitted down the optic nerve sheaths. This then compresses the central retinal vein as it traverses the intervaginal space.6 Others believe that the raised pressure within the retinal vasculature is due to raised intracranial pressure being transmitted to the intracranial venous channels and then to the orbital veins.7
Another theory is that the sudden rise in intracranial pressure is transmitted down the optic nerve sheath to the lamina cribosa sclerae, where it occludes the retinal and choroidal anastomoses and consequently causes increased pressure within the retinal vasculature.8
The influence of intracranial hypertension on the terminal subarachnoid space of the optic nerve sheath induces damage to the border tissue of El-schnig, the border tissue of Jacoby, the intermediary tissue of Kuhnt, the peripapillary retina, and the inner limiting membrane.9 The blood escapes into the vitreous through this peripapillary region.
In our case, the infant had a persistent patent hyaloid artery and had associated raised intracranial pressure secondary to an intraventricular bleed. The vitreous hemorrhage was centered around the optic disc and the persistent hyaloid artery, so we believe that the raised intracranial pressure led to increased pressure within the retinal vasculature and hyaloid vessel from a Terson-like mechanism leading to bleeding from the hyaloid artery. However, there were no retinal hemorrhages noted on examination. The vitreous hemorrhage led to an organized ochre membrane that we believed was unlikely to clear within the critical period of visual development and hence decided to go ahead with vitrectomy.
Neonatal eyes are normally hypermetropic and they become gradually emmetropic with increasing age. This process is called emmetropization and is sensitive to visual disturbance. Altered visual experience can cause myopia, and emmetropization of the human eye is a vision-dependent phenomenon.10 Prematurity and ROP are also associated with myopia due to arrested development of the anterior segment.11
Our patient developed high myopia in the affected eye. The unilateral nature of the high myopia may indicate a unilateral disturbance of emmetropization or ocular growth due to the presence of vitreous hemorrhage or intervention with vitrectomy.
It is believed that in infants with media opacities (eg, congenital cataract) surgery undertaken within the first 6 weeks has a better visual outcome than later surgery. Our patient was a premature infant born at 28 weeks who was operated on at near term, and so was within this critical time frame. However, his visual behavior remained poor, which was probably related to optic atrophy, and high myopia developed in the eye that had surgery. Previous reports have also noted poor visual outcomes in cases of persistent hyaloid vessels.2
This article reports a rare scenario of Terson syndrome in a premature infant with a persistent hyaloid artery. The infant went on to have a vitrectomy to clear the ocular media and prevent deprivation amblyopia. However, the infant had a poor visual outcome and developed high myopia, demonstrating failure of emmetropization unilaterally.
- Duke-Elder S. Normal and abnormal development: congenital deformities, vol. 3, part 2. In: Duke Elder S, ed. System of Ophthalmology. London: Henry Kimpton; 1964:761–782.
- Gonçalves A, Cruysberg JRM, Draaijer RW, et al. Vitreous hemorrhage and other ocular complications of a persistent hyaloid artery. Doc Ophthalmol. 1996;92:55–59. doi:10.1007/BF02583277 [CrossRef]
- Onder F, Cossar CB, Gültan E, Kural G. Vitreous hemorrhage from the persistent hyaloid artery. J AAPOS. 2000;4:190–191.
- Schloff S, Mullaney PB, Armstrong DC, et al. Retinal findings in children with intracranial hemorrhage. Ophthalmology. 2002;109:1472–1476. doi:10.1016/S0161-6420(02)01086-2 [CrossRef]
- Medele RJ, Stummer W, Mueller AJ, Steiger HJ, Reulen HJ. Terson’s syndrome in subarachnoid hemorrhage and severe brain injury accompanied by acutely raised intracranial pressure. J Neurosurg. 1998;88:851–854. doi:10.3171/jns.1998.88.5.0851 [CrossRef]
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- Hedges TR Jr, Walsh FB. Optic nerve sheath and subhyaloid hemorrhage as a complication of angiocardiography. Arch Ophthalmol. 1955;54:425–427. doi:10.1001/archopht.1955.00930020431015 [CrossRef]
- Ou RJ. Terson syndrome. Medscape Reference Drugs, Conditions and Procedures. Available at: http://emedicine.medscape.com/article/1227921-overview?a0101. Accessed April 20, 2011.
- Ogawa T, Kitaoka T, Dake Y, et al. Terson syndrome: a case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology. 2001;108:1654–1656. doi:10.1016/S0161-6420(01)00673-X [CrossRef]
- Rabin J, Van Sluyters RC, Malach R. Emmetropization: a vision dependent phenomenon. Invest Ophthalmol Vis Sci. 1981;20:561–564.
- Fledelius HC. Pre-term delivery and subsequent ocular development. Acta Ophthalmol Scand. 1996;74:297–300. doi:10.1111/j.1600-0420.1996.tb00096.x [CrossRef]