Superficial and Deep Capillary Plexus Nonperfusion in Nonaccidental Injury on OCTA

Abstract

Purpose:

To report OCTA findings in a case of nonaccidental injury (NAI).

Methods:

Retrospective review of a clinical case.

Results:

A 5-year-old White child with a history of NAI at age 1 year presented with reduced vision in the left eye resulting from a closed funnel retinal detachment. The right eye had optic nerve pallor, peripheral vascular attenuation, and leakage. Optical coherence tomography angiography (OCTA) showed significant parafoveal attenuation of the superficial vascular plexus, intermediate capillary plexus, and deep capillary plexus. This correlated with inner and middle retinal layer thinning temporal to the fovea and preservation of the ellipsoid zone. The peripapillary vascular plexus was preserved. Laser photocoagulation was performed to the nonperfused peripheral retina, and intravitreal bevacizumab was injected. Attenuation of the superficial, intermediate, and deep capillary plexuses might represent chronic ischemic retinal changes from traumatic injury to the vitreoretinal interface and inner retina in NAI.

Conclusions:

OCTA identified nonperfusion of the superficial and deep vascular plexuses as late sequelae of NAI. Traumatic injuries to the vitreoretinal interface in NAI might lead to inner retinal ischemia and atrophy with vascular attenuation present on OCTA.

Introduction

Nonaccidental injury (NAI) is the most common cause of trauma-related death in childhood. ¹ Manifestations can include any combination of subdural hemorrhage, subarachnoid hemorrhage, retinal hemorrhage, or encephalopathy. ² Retinal hemorrhages, presumed to arise from the traumatic whiplash effect on the vitreoretinal interface, have been reported in 83% of cases. ³ Optical coherence tomography (OCT) of eyes with NAI has identified the presence of epiretinal membrane (ERM), macular hole (MH), perimacular folds, and inner retinoschisis, with the latter 2 regarded as highly specific for poor visual outcomes.^4,5 However, the presence of vascular nonperfusion in eyes with NAI has been limited to the peripheral retina using fluorescein angiography (FA) but has not been described in the more visually significant macula. ⁶ The current case documents OCT angiography (OCTA) findings of capillary nonperfusion in the macula in a patient with history of NAI.

Case Report

A 5-year old White child with history of NAI at age 1 year was referred for reduced vision and a new afferent pupillary defect in the left eye. In addition to ocular findings, he sustained traumatic cortical encephalopathy with subsequent global developmental delays. He had no history of prematurity or birth-related medical issues. The patient had been followed by a local optometrist every 6 months with previously documented bilateral optic nerve pallor and an ERM in the left eye.

On our initial visual examination, the patient grimaced to light in the right eye and had no light perception in the left eye. The intraocular pressure was 21 mm Hg and 17 mm Hg in the right eye and left eye, respectively. An examination under anesthesia showed a total funnel-shaped retinal detachment (RD) in the left eye via ultrasound B-scan. This was deemed inoperable at the time and was to be kept under observation. The fundus in the right eye had optic nerve pallor and peripheral vascular attenuation (Figure 1A). FA of the right eye showed peripheral nonperfusion and areas of vascular leakage (Figure 1, B and C). Spectral-domain OCT (Spectralis HRA+OCT with Flex module, Heidelberg Engineering) showed significant thinning of the inner and middle retinal layers temporal to the fovea. In turn, the outer retinal ellipsoid zone (EZ) appeared to be relatively intact (Figure 2, A and B). OCTA showed significant attenuation of the superficial vascular and deep capillary plexuses temporal to the fovea (Figure 2, C and D). Laser photocoagulation to the nonperfused peripheral retina was performed, and intravitreal bevacizumab injection was given in the right eye.

Figure 1.

(A) Fundus photograph shows peripheral vascular attenuation and optic nerve pallor. (B and C) Fluorescein angiography shows focal areas of distal hypoperfusion and vascular leakage.

Figure 2.

(A and B) Spectral-domain optical coherence tomography images show significant inner and middle retinal layer thinning with preservation of the ellipsoid zone layer. Red-free images show a demarcation line temporal to the fovea, suggestive of a transition between the perfused and hypoperfused retina. (C and D) Optical coherence tomography angiography shows significant vessel attenuation of the superficial and deep vascular complexes.

Conclusions

The current report characterizes nonperfusion of the parafoveal superficial vascular plexus, intermediate vascular plexus, and deep capillary plexus using OCTA in a patient with history of NAI. Macular findings on OCT in eyes with NAI have included MH, ERM, internal limiting membrane traction, perimacular folds, and retinoschisis.^4,5 These macular changes might result from direct mechanical trauma or secondary to vitreoretinal traction, but less likely from an ischemic insult.

Our group previously reported peripheral, but not macular, retinal nonperfusion in NAI using FA. ⁶ These changes included truncation of the vasculature and chorioretinal scarring temporal to the macula, which correlated with decreased CD31 vascular lumen markers in cadaver eyes. Some have suggested the presence of preretinal neovascularization as sequelae from NAI, although this has been contested in histopathologic correlations.^6,7 Multimodal imaging that includes FA is essential in these patients because peripheral nonperfusion and vascular leakage might lead to neovascularization, vitreoretinal traction, and potentially an RD. ⁸ We suspect this occurred in our patient’s left eye. In addition, electroretinography with negative waveforms can be a tool for predicting poor visual outcomes. ⁹ To our knowledge, the current report is the first OCTA characterization of vascular nonperfusion in the macula in an eye with NAI.

Perifoveal vascular microanatomy has been mapped by OCTA. ¹⁰ The deep capillary circulation terminates at the foveal avascular zone (FAZ), while the superficial circulation terminates in the parafoveal area away from the FAZ. ¹⁰ In our patient, the ischemia was affecting all retinal layers, but in varying degrees. Because the perifoveal area in our patient showed a faint signal compared with the total obliteration found in the superficial layers, it is possible that the ischemic insult could have occurred more proximally. This correlated with the OCT B-scan showing thinning of the inner retinal layers with a relatively intact middle retina and EZ.

The mechanism of retinal ischemia in eyes with NAI might be multifactorial and is manifested by multilayered microvascular injury. The superficial vascular plexus attenuation and inner retinal ischemia in our patient might be explained by microvascular injury from trauma-induced tractional forces affecting the vitreoretinal interface. Acute macular changes in NAI have been described with inner retinoschisis, possibly related to tractional injury.^4,5 Traumatic injuries are also suggested to be the cause of preretinal hemorrhages in eyes with NAI. It is possible that inner retinal manifestations of NAI presents acutely with inner retinal edema and lamellar inner retinoschisis and chronically with inner retinal atrophy and superficial vascular plexus attenuation. Therefore, severe vitreoretinal traction might have an injurious effect on the inner retina in eyes with NAI. Additional mechanisms, such as intravascular thrombosis, stasis, and nonperfusion from intracranial pressure, could also be contributory. ¹¹ This might serve to further expand the spectrum of chronic retinal pathology in eyes with NAI.

In conclusion, OCTA might help characterize chronic nonperfusion of the superficial vascular plexus, intermediate vascular plexus, and deep capillary plexus in an eye with NAI. The more severe changes in the superficial vasculature correlate with inner retinal atrophy. These changes might represent chronic manifestation of traumatic injury at the vitreoretinal interface.