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Research Letters |

Subclinical Photoreceptor Disruption in Response to Severe Head Trauma FREE

Kimberly E. Stepien, MD; Wanda M. Martinez, MD, PhD; Adam M. Dubis, BA; Robert F. Cooper, BS; Alfredo Dubra, PhD; Joseph Carroll, PhD
[+] Author Affiliations

Author Affiliations: Departments of Ophthalmology (Drs Stepien, Martinez, and Carroll), Cell Biology, Neurobiology, and Anatomy (Mr Dubis and Dr Carroll), and Biophysics (Dr Carroll), Medical College of Wisconsin, and Department of Biomedical Engineering, Marquette University (Mr Cooper), Milwaukee; and Flaum Eye Institute, University of Rochester, Rochester, New York (Dr Dubra).


Arch Ophthalmol. 2012;130(3):400-402. doi:10.1001/archopthalmol.2011.1490.
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Commotio retinae is a transient opacification of the retina due to outer retinal disruption occurring in a contrecoup fashion after blunt trauma.1,2 Histological studies in animals and humans after ocular blunt trauma have revealed that disruption occurs at the level of the photoreceptor outer segments and retinal pigment epithelium.2,3 Recent reports using optical coherence tomography (OCT) have shown detectable disruption at the level of the photoreceptor inner segment/outer segment junction and retinal pigment epithelium46 and that these changes may be reversible over time with restoration of normal outer retinal architecture.5 However, the resolution of existing OCT technology may not be sensitive enough to detect photoreceptor disruption. Adaptive optics (AO) imaging systems enable cellular-resolution imaging of the human retina, and there is a growing number of cases where deficits have been visible on AO images but not on OCT. Herein, we report a case of subclinical photoreceptor disruption after head trauma as seen by an AO scanning ophthalmoscope (AOSO) but not apparent clinically or on spectral-domain OCT (SD-OCT).

A 43-year-old man described a 5-year history of a stable, crescent-shaped purple scotoma nasal to central fixation in his right eye that developed after an industrial accident in which he sustained significant head and body trauma. A complete ophthalmic examination revealed best-corrected visual acuity of 20/20 OU and no remarkable fundus findings or abnormalities. Fluorescein angiography and SD-OCT (Spectralis SD-OCT; Heidelberg Engineering) findings were unremarkable (Figure 1). Humphrey visual field 10-2 testing and microperimetry revealed a small nonspecific area of functional vision loss near fixation in the right eye. Images of the photoreceptor mosaic near the fovea were acquired using a newly developed AOSO. Images were processed and registered using custom MatLab software (MathWorks). While foveal cone density was normal, the AOSO images revealed a well-defined crescent-shaped area of photoreceptor disruption just temporal to the fovea (Figure 2A, large arrows). Other focal areas of photoreceptor irregularities were also seen superior, temporal, and inferotemporal to the fovea (Figure 2A, small arrows). Both cone and rod photoreceptors were visualized with this AOSO imaging, and both cell types appeared to be disrupted (Figure 2A and B).

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Figure 1. Clinical imaging of the right eye. A, Color fundus photograph shows no macular abnormalities. B, Late-frame fluorescein angiogram shows no window defect, staining, or leakage. White box indicates the area imaged by the adaptive optics scanning ophthalmoscope as seen in Figure 2. C, Spectralis spectral-domain optical coherence tomographic horizontal scan through the fovea shows no outer retinal abnormalities. Area between arrows indicates the region imaged by the adaptive optics scanning ophthalmoscope as seen in Figure 2.

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Figure 2. Disrupted photoreceptor mosaic of the macula in the right eye. A, Adaptive optics scanning ophthalmoscope montage shows a large, crescent-shaped area of photoreceptor disruption (edges indicated by large arrows) temporal to the fovea. Other areas of photoreceptor disruption are also present (small arrows). The foveal center was not imaged (solid white rectangle). B, Magnified view of a patch of retina 1° temporal from the fovea, centered on an area of significant photoreceptor disruption. C, Magnified view of a patch of retina 1° nasal from the fovea, showing a regularly packed cone photoreceptor mosaic. D, Image from a healthy control subject, about 1° temporal from the fovea. Scale bars = 50 μm.

The AOSO detected photoreceptor disruption resulting from head trauma and not apparent clinically or by other standard imaging modalities, including SD-OCT. Restoration of the outer retinal appearance in SD-OCT has been reported after commotio retinae,5 suggesting recovery of the outer retinal structure. Our data demonstrate that photoreceptor disruption may still exist. The SD-OCT axial resolution is likely not sensitive enough to reveal the full extent of photoreceptor disruption that may occur after ocular or head trauma. The AOSO imaging may prove useful in improved detection and understanding of photoreceptor involvement in ocular or head trauma. In addition, patients with traumatic brain injury often report visual symptoms. The AOSO may be of value to help differentiate retinal vs cortical contributions to vision loss in these patients.

Correspondence: Dr Stepien, Department of Ophthalmology, The Eye Institute, Medical College of Wisconsin, 925 N 87th St, Milwaukee, WI 53226 (kstepien@mcw.edu).

Author Contributions: Dr Stepien had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Financial Disclosure: None reported.

Funding/Support: This work was supported by the Clinical and Translational Science Institute and the Biotechnology Innovation Center, Medical College of Wisconsin, Clinical and Translational Science Award UL1 RR 031973 and grants EY017607, EY001931, and EY014537 from the National Institutes of Health, the Thomas M. Aaberg Sr Retina Research Fund, the E. Matilda Ziegler Foundation for the Blind, the R. D. and Linda Peters Foundation, and Research to Prevent Blindness. Dr Dubra holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. Dr Carroll is the recipient of a Career Development Award from Research to Prevent Blindness. This investigation was conducted in a facility constructed with support from Extramural Research Facilities Improvement Program grant C06 RR-RR016511 from the National Center for Research Resources, National Institutes of Health.

Previous Presentation: This paper was presented as a poster at the 2011 Annual Meeting of the Association for Research in Vision and Ophthalmology; May 3, 2011; Fort Lauderdale, Florida.

Liem AT, Keunen JE, van Norren D. Reversible cone photoreceptor injury in commotio retinae of the macula.  Retina. 1995;15(1):58-61
PubMed   |  Link to Article
Sipperley JO, Quigley HA, Gass DM. Traumatic retinopathy in primates: the explanation of commotio retinae.  Arch Ophthalmol. 1978;96(12):2267-2273
PubMed   |  Link to Article
Mansour AM, Green WR, Hogge C. Histopathology of commotio retinae.  Retina. 1992;12(1):24-28
PubMed   |  Link to Article
Bradley JL, Shah SP, Manjunath V, Fujimoto JG, Duker JS, Reichel E. Ultra–high-resolution optical coherence tomographic findings in commotio retinae.  Arch Ophthalmol. 2011;129(1):107-108
PubMed   |  Link to Article
Itakura H, Kishi S. Restored photoreceptor outer segment in commotio retinae.  Ophthalmic Surg Lasers Imaging. 2011;42 online:e29-e31
PubMed  |  Link to Article
Seider MI, Lujan BJ, Gregori G, Jiao S, Murray TG, Puliafito CA. Ultra-high resolution spectral domain optical coherence tomography of traumatic maculopathy.  Ophthalmic Surg Lasers Imaging. 2009;40(5):516-521
PubMed   |  Link to Article

Figures

Place holder to copy figure label and caption
Graphic Jump Location

Figure 1. Clinical imaging of the right eye. A, Color fundus photograph shows no macular abnormalities. B, Late-frame fluorescein angiogram shows no window defect, staining, or leakage. White box indicates the area imaged by the adaptive optics scanning ophthalmoscope as seen in Figure 2. C, Spectralis spectral-domain optical coherence tomographic horizontal scan through the fovea shows no outer retinal abnormalities. Area between arrows indicates the region imaged by the adaptive optics scanning ophthalmoscope as seen in Figure 2.

Place holder to copy figure label and caption
Graphic Jump Location

Figure 2. Disrupted photoreceptor mosaic of the macula in the right eye. A, Adaptive optics scanning ophthalmoscope montage shows a large, crescent-shaped area of photoreceptor disruption (edges indicated by large arrows) temporal to the fovea. Other areas of photoreceptor disruption are also present (small arrows). The foveal center was not imaged (solid white rectangle). B, Magnified view of a patch of retina 1° temporal from the fovea, centered on an area of significant photoreceptor disruption. C, Magnified view of a patch of retina 1° nasal from the fovea, showing a regularly packed cone photoreceptor mosaic. D, Image from a healthy control subject, about 1° temporal from the fovea. Scale bars = 50 μm.

Tables

References

Liem AT, Keunen JE, van Norren D. Reversible cone photoreceptor injury in commotio retinae of the macula.  Retina. 1995;15(1):58-61
PubMed   |  Link to Article
Sipperley JO, Quigley HA, Gass DM. Traumatic retinopathy in primates: the explanation of commotio retinae.  Arch Ophthalmol. 1978;96(12):2267-2273
PubMed   |  Link to Article
Mansour AM, Green WR, Hogge C. Histopathology of commotio retinae.  Retina. 1992;12(1):24-28
PubMed   |  Link to Article
Bradley JL, Shah SP, Manjunath V, Fujimoto JG, Duker JS, Reichel E. Ultra–high-resolution optical coherence tomographic findings in commotio retinae.  Arch Ophthalmol. 2011;129(1):107-108
PubMed   |  Link to Article
Itakura H, Kishi S. Restored photoreceptor outer segment in commotio retinae.  Ophthalmic Surg Lasers Imaging. 2011;42 online:e29-e31
PubMed  |  Link to Article
Seider MI, Lujan BJ, Gregori G, Jiao S, Murray TG, Puliafito CA. Ultra-high resolution spectral domain optical coherence tomography of traumatic maculopathy.  Ophthalmic Surg Lasers Imaging. 2009;40(5):516-521
PubMed   |  Link to Article

Correspondence

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