Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Optical Coherence Tomography Angiography of Retinal Perfusion in Chiasmal Compression

Tomoaki Higashiyama, MD; Yusuke Ichiyama, MD; Sanae Muraki, MD; Yasuhiro Nishida, MD; Masahito Ohji, MD

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the retinal perfusion in patients with chiasmal compression using optical coherence tomography angiography (OCTA).

PATIENTS AND METHODS:

Retinal perfusion was evaluated using OCT angiograms in eight eyes of four patients with visual field (VF) defects due to chiasmal compression treated by tumor resection. The retinal perfusion in the area corresponding to the quadrants of the VF defects was investigated in each image. The vessel density was defined as the percentage area occupied by the vessels in the image.

RESULTS:

The decreased peripapillary retinal perfusion correlated with the quadrants of the VF defects on OCT angiograms in all patients. The binarized vessel density decreased, corresponding to the degree of VF defects in all patients.

CONCLUSIONS:

A decrease in peripapillary retinal perfusion correlates with the quadrants of the VF defects due to chiasmal compression. This decrease can be noninvasively measured by OCTA.

[Ophthalmic Surg Lasers Imaging Retina. 2016;47:724–729.]

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the retinal perfusion in patients with chiasmal compression using optical coherence tomography angiography (OCTA).

PATIENTS AND METHODS:

Retinal perfusion was evaluated using OCT angiograms in eight eyes of four patients with visual field (VF) defects due to chiasmal compression treated by tumor resection. The retinal perfusion in the area corresponding to the quadrants of the VF defects was investigated in each image. The vessel density was defined as the percentage area occupied by the vessels in the image.

RESULTS:

The decreased peripapillary retinal perfusion correlated with the quadrants of the VF defects on OCT angiograms in all patients. The binarized vessel density decreased, corresponding to the degree of VF defects in all patients.

CONCLUSIONS:

A decrease in peripapillary retinal perfusion correlates with the quadrants of the VF defects due to chiasmal compression. This decrease can be noninvasively measured by OCTA.

[Ophthalmic Surg Lasers Imaging Retina. 2016;47:724–729.]

Introduction

Chiasmal compression due to tumors causes visual function disorders such as visual loss and visual field (VF) defects.1,2 These visual function disorders depend on the degree of structural and functional damage because chiasmal compression causes retrograde degeneration to retinal ganglion cells (RGC) and their axons.3 In some cases, the visual function damage cannot be reversed, even after tumor resection.2,3

Optical coherence tomography (OCT) and electroretinograms have been used to evaluate the retinal structural and functional damage due to chiasmal compression.3,8 A previous study using OCT reported that the mean ganglion cell complex (GCC) thickness and retinal nerve fiber layer (RNFL) thickness in eyes with chiasmal compression were significantly thinner than in normal eyes.5 Because of chiasmal compression, RNFL thicknesses using OCT and multifocal pattern electroretinogram amplitudes were significantly smaller in eyes with temporal hemianopia than in normal eyes.6 However, to the best of our knowledge, evaluation of retinal perfusion with chiasmal compression, including fluorescein angiography, has not been previously reported.

Although conventional OCT is useful for evaluating the retinal structure, it cannot evaluate retinal perfusion.9 Doppler OCT, calculated from the Doppler frequency shift of backscattered light, has been previously used to measure total retinal perfusion.10 However, Doppler OCT can only measure large vessels and is not sensitive enough to evaluate small vessels.11 Because OCT angiography (OCTA) can discriminate the blood flow areas, it was recently developed for mapping ocular perfusion, including capillaries.12,16 A previous study using OCTA for diabetic retinopathy reported that OCT angiograms can clearly resolve retinal capillaries, retinal nonperfusion areas, and microaneurysms in patients.16 Moreover, OCTA is useful for evaluating the perfusion of not only the macula, but also the peripapillary retina,12,17,19 and a previous study reported that the peripapillary retinal perfusion was reduced in glaucoma.19 In the following study, therefore, we investigated the retinal perfusion corresponding to the quadrants of the VF defects due to chiasmal compression in the disc and macula using OCTA.

Patients and Methods

Patients

Eight eyes of four patients (three female, one male) with VF defects due to chiasmal compression even after tumor resection were included in this observational, cross-sectional study. The patients were evaluated with OCTA in the Department of Ophthalmology, Shiga University of Medical Science Hospital, from July 2015 to August 2015. All OCTA was taken after tumor resection. This study was approved by the institutional review board of the Shiga University of Medical Science. The study was conducted in accordance with the tenets of the Declaration of Helsinki. Written informed consent was obtained from each patient in this study. All patients had VF defects even after surgery for chiasmal tumors. Before treatment, magnetic resonance imaging (MRI) examinations were performed to confirm chiasmal compression due to tumors. The patients underwent ophthalmological examinations including measurements of best-corrected visual acuity (BCVA), critical flicker frequency, OCT, and VF testing. VF testing was performed with Goldmann perimetry (GP; Haag-Streit, Bern, Switzerland) or the Humphrey Field Analyzer (HFA; Carl-Zeiss Meditec, Dublin, CA) using the 30-2 Swedish Interactive Threshold Algorithm (SITA)-fast program. VF testing using the HFA was excluded if the false-positives, false-negatives, or fixation losses of the test were more than 30%.

OCTA

The OCT angiograms were obtained using spectral-domain OCT (RTVue XR Avanti; Optovue, Fremont, CA). Because the instrument can discriminate the motion of scattering particles such as red blood cells, the vessels could be clearly shown in the images without fluorescein angiography.

We used OCT angiograms centered on the disc (4.5 mm × 4.5 mm) and the macula (6 mm × 6 mm), using a split-spectrum amplitude-decorrelation angiography algorithm. Different layers are shown in the OCT angiogram using this instrument. We used the radial peripapillary capillary images in the disc and the superficial images in the macula and evaluated the relationships between the retinal perfusion in the images and the quadrants of the VF defects due to chiasmal compression. The OCT angiograms were binarized to clearly resolve the microvasculature. We measured the vessel density, which was defined as the percentage area occupied by the vessels in the images using Image J software (National Institutes of Health, Bethesda, MD; http://rsbweb.nih.gov/ij/index.html).20 The characters “angio FLOW” in each image were included in the measurements. The vessel densities of both eyes were measured in the same binarized setting and compared in each patient.

GCC

The GCC thickness of the macula was measured with RTVue XR Avanti software. GCC thickness was defined as the distance from the inner limiting membrane to the outer boundary of the inner plexiform layer. The RTVue XR Avanti software produced a GCC significance map in which GCC was compared with normal eyes. Thicknesses and losses were shown in red and yellow, respectively.

Results

The characteristics of the patients are shown in Table 1. The mean age of the patients was 52.3 years ± 13.1 years (mean ± standard deviation, range: 36 years to 67 years). The chiasmal tumors of the patients were histopathologically diagnosed with pituitary adenoma in two cases (Cases 1 and 4), craniopharyngioma in one case (Case 2), and meningioma in one case (Case 3). The tumor resection surgeries were performed twice in Case 1 and once in Cases 2, 3, and 4. The mean postoperative period was 18.8 months ± 14.5 months (range: 6 months to 40 months).


Characteristics of Patients

Table 1:

Characteristics of Patients

The peripapillary retinal perfusion decreases correlated with the quadrants of the VF defects on OCT angiograms in all patients (Figures 1 to 4). The vessel densities in the disc areas are shown in Table 2. The decreased vessel densities in the disc areas correlated with the degrees of VF defects in all patients. However, a correlation between the retinal perfusion and the quadrants of the VF defects was not found on OCT angiograms of the macular area. A correlation between the vessel density in the macular area and the degree of VF defect was also not found (Table 2). In addition, the GCC thicknesses in the retina correlated with VF defects were decreased in all eyes.


Visual field (VF) findings, optical coherence tomography (OCT) angiograms, and ganglion cell complex (GCC) significance maps in Case 1. A 36-year-old female patient with pituitary adenoma. The patient underwent tumor resection 17 months prior to this study. The pattern deviation of the Humphrey Field Analyzer (A). A lower nasal VF defect was detected in the right eye. Original images of OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the upper temporal retina (arrowheads) in the right eye. Binarized images of OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the upper temporal retina (arrowheads) corresponding to the quadrants of the VF defects in the right eye. Original OCT angiograms of the macula of the right eye (F) and of the left eye (G). Binarized OCT angiograms of the macula of the right eye (H) and of the left eye (I). The retinal perfusion did not decrease in the retina corresponding to the quadrants of the VF defects in the right eye. GCC significance maps of the right eye (J) and of the left eye (K). The decreased GCC thickness of the upper retina of the right eye correlated with the VF defect.

Figure 1.

Visual field (VF) findings, optical coherence tomography (OCT) angiograms, and ganglion cell complex (GCC) significance maps in Case 1. A 36-year-old female patient with pituitary adenoma. The patient underwent tumor resection 17 months prior to this study. The pattern deviation of the Humphrey Field Analyzer (A). A lower nasal VF defect was detected in the right eye. Original images of OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the upper temporal retina (arrowheads) in the right eye. Binarized images of OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the upper temporal retina (arrowheads) corresponding to the quadrants of the VF defects in the right eye. Original OCT angiograms of the macula of the right eye (F) and of the left eye (G). Binarized OCT angiograms of the macula of the right eye (H) and of the left eye (I). The retinal perfusion did not decrease in the retina corresponding to the quadrants of the VF defects in the right eye. GCC significance maps of the right eye (J) and of the left eye (K). The decreased GCC thickness of the upper retina of the right eye correlated with the VF defect.


Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 2. A 67-year-old female patient with craniopharyngioma. The patient underwent tumor resection 12 months prior to this study. VF findings of Goldmann perimetry (A). Temporal VF defects were detected in both eyes and the VF defect in the left eye was more severe than the right eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was especially decreased in the nasal retina corresponding to the quadrants of the VF defects in the left eye.

Figure 2.

Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 2. A 67-year-old female patient with craniopharyngioma. The patient underwent tumor resection 12 months prior to this study. VF findings of Goldmann perimetry (A). Temporal VF defects were detected in both eyes and the VF defect in the left eye was more severe than the right eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was especially decreased in the nasal retina corresponding to the quadrants of the VF defects in the left eye.


Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 3. A 57-year-old female patient with meningioma. The patient underwent tumor resection 40 months prior to this study. VF findings of Goldmann perimetry (A). A lower nasal VF defect was detected in the left eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the upper temporal retina (arrowhead) in the left eye. Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the upper temporal retina (arrowhead) corresponding to the quadrants of the VF defects in the left eye.

Figure 3.

Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 3. A 57-year-old female patient with meningioma. The patient underwent tumor resection 40 months prior to this study. VF findings of Goldmann perimetry (A). A lower nasal VF defect was detected in the left eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the upper temporal retina (arrowhead) in the left eye. Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the upper temporal retina (arrowhead) corresponding to the quadrants of the VF defects in the left eye.


Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 4. A 49-year-old male patient with pituitary adenoma. He underwent tumor resection 6 months prior to this study. Pattern deviation using the Humphrey Field Analyzer (A). The VF testing showed an upper temporal VF defect in the right eye and a temporal and lower nasal VF defect in the left eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the retina (arrowhead) in both eyes. Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the retina (arrowhead) corresponding to the quadrants of the VF defects in both eyes.

Figure 4.

Visual field (VF) findings and optical coherence tomography (OCT) angiograms in Case 4. A 49-year-old male patient with pituitary adenoma. He underwent tumor resection 6 months prior to this study. Pattern deviation using the Humphrey Field Analyzer (A). The VF testing showed an upper temporal VF defect in the right eye and a temporal and lower nasal VF defect in the left eye. OCT angiograms of the disc of the right eye (B) and of the left eye (C). The retinal perfusion was decreased in the retina (arrowhead) in both eyes. Binarized OCT angiograms of the disc of the right eye (D) and of the left eye (E). The retinal perfusion was decreased in the retina (arrowhead) corresponding to the quadrants of the VF defects in both eyes.


Visual Field Defects and Vessel Densities

Table 2:

Visual Field Defects and Vessel Densities

One representative case (Case 1) of a 36-year-old woman is shown in Figures 1 and 5. Her BCVA was 20/32 in the right eye and 20/13 in the left eye before the first surgery. The critical flicker frequency value was 12 Hz in the right eye and 40 Hz in the left eye. A relative afferent pupillary defect was detected in the right eye. A lower nasal VF defect was found in the right eye. The VF defect remained even after tumor resection in the right eye (Figure 1A). OCTA of the disc showed decreased retinal perfusion in the upper temporal retina that corresponded to the quadrants of the VF defects in the right eye (Figures 1A and 1B). The vessel density in the disc area was 38.7% in the right eye and 54.5% in the left eye. OCT angiograms of the macula showed no decrease in the retinal perfusion correlating with the quadrants of the VF defects (Figures 1F and 1G). The vessel density in the macula area was 25.8% in the right eye and 26.2% in the left eye. GCC thickness in the upper retina of the right eye correlated with the VF defects (Figure 1J).

Discussion

Using OCT angiograms, we showed that retrograde decreases in peripapillary retinal perfusion correlated with the quadrants of the VF defects due to chiasmal compression. The evaluation of the retinal perfusion, including fluorescein angiography, has not been previously reported. Because visual information is transferred along axons of RGCs within the nerve fiber layer of the retina, chronic damage due to chiasmal compression often leads to nerve fiber layer defects.21,22 Previous studies reported that the thicknesses of the GCC and RNFL in the retina of patients with chiasmal compression were significantly thinner than those in controls.5,6 OCT angiograms in our study showed decreases of the peripapillary retinal perfusion correlating with the quadrants of the VF defects. Chiasmal damage due to tumors leads to decreases of not only retinal structures but also peripapillary retinal perfusion.

In the present study, decreases in peripapillary vessel densities in disc areas correlated with the degrees of VF defects in all patients. Using OCTA, Liu et al. compared the peripapillary vessel densities of 12 glaucomatous eyes and 12 normal eyes.19 The peripapillary vessel densities were defined as the percentage of areas occupied by the vessels of the regions under study. The peripapillary vessel density was highly correlated with mean deviation and pattern standard deviation of VF testing in patients with glaucoma. Consistent with this previous study, our present study showed that the decreases in peripapillary vessel densities correlated with the degrees of VF defects in all patients with chiasmal compression.

In the present study, the GCC thicknesses in the retina correlated with VF defects were decreased. Because GCC loss suggests the degeneration of RGC and optic nerve fibers, VF defects could not recover to normal levels despite tumor resection in the patients with GCC loss. A previous study suggested that preoperative GCC thickness might be useful in predicting the VF after surgery.5 Our present study showed that decreases in not only the GCC thickness, but also the peripapillary retinal perfusion in the retina, correlated with VF defects. Preoperative peripapillary retinal perfusion may, therefore, be useful in predicting the VF after surgery, although this possibility needs to be confirmed with future studies using preoperative OCTA.

The present study has some limitations. First, VF testing in this study was performed with GP in two cases and with HFA in two cases. The measurement areas of the OCT angiograms centered on the disc and the macula were smaller than those of the visual field testing. OCT angiograms could be evaluated by the quadrants of the VF defects in chiasmal compression. Moreover, because many previous studies have reported that HFA using the SITA program and GP produced similar results in the evaluation of the VF due to chiasmal disorders,23,24 the limitation may not be significant. Second, the sample size of the current study was small. Only eight eyes of four patients were studied. Third, the vessel densities were not compared among different patients because the density setting in the binarized mode of the OCT angiograms were individually chosen. However, the vessel densities could be compared between both eyes of each patient because the densities were measured using the same binarized settings. Fourth, correlations between the retinal perfusion in the macula and the quadrants of the VF defects were not determined in our study. The retinal nerve fibers of both the nasal and temporal halves in the macula contained temporal discs unlike the fibers in the peripheral retina, so the complexity of the retinal nerve fiber in the macula may be related to this observation.

In conclusion, OCTA can noninvasively detect correlations between decreases of the peripapillary retinal perfusion and the quadrants of the VF defects. There was a correlation of decreased peripapillary vessel densities in disc areas with the degrees of VF defects in all patients. We have shown that a retrograde decrease in peripapillary retinal perfusion correlates with the quadrants of the VF defects due to chiasmal compression.

References

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Characteristics of Patients

CaseAge (Years)SexChiasmal TumorPostoperative Periods (Months)Visual Field Defect

136FPituitary adenoma17R: lower nasal
267FCraniopharyngioma12B: temporal (R < L)
357FMeningioma40L: lower nasal
449MPituitary adenoma6R: upper temporal, L: temporal and lower nasal

Visual Field Defects and Vessel Densities

CaseVisual Field DefectVessel Density in Disc (%)Vessel Density in Macula (%)
RLRL

1R: lower nasal38.754.525.826.2
2B: temporal (R < L)49.322.019.732.6
3L: lower nasal54.447.621.829.2
4R: upper temporal L: temporal and lower nasal33.416.428.213.0
Authors

From the Department of Ophthalmology, Shiga University of Medical Science, Otsu, Japan (TH, YI, SM, MO); and the Clinical Medical Education Center, Shiga University of Medical Science, Otsu, Japan (YN).

Dr. Higashiyama has received grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#15K10862) and personal fees from Senju Pharmaceutical, Pfizer, and Japan Ophthalmologists Association of Shiga. Dr. Ichiyama has received grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#15K10862). Dr. Muraki has received grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#15K10862) and personal fees from Santen Pharmaceutical and Senju Pharmaceutical. Dr. Nishida has received personal fees from Japan Ophthalmologists Association of Fukui, Japan Ophthalmologists Association, Hikone Medical Association, Kinki Strabismus and Amblyopia Afternoon Seminar, and the Shiga Physicians Association. Dr. Ohji has received grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#15K10862) and personal fees from Alcon Japan, Novartis, Santen Pharmaceutical, Senju Pharmaceutical, Bayer, Carl Zeiss Japan, Otsuka Pharmaceutical, Shionogi & Co., MSD, Kowa Pharmaceutical Company, Pfizer Japan, and Sanwa Kagaku Institute.

Address correspondence to Tomoaki Higashiyama, MD, Department of Ophthalmology, Shiga University of Medical Science, Seta, Tsukinowa-cho, Otsu, Shiga 520-2192, Japan; email: higashi@belle.shiga-med.ac.jp.

Received: December 24, 2015
Accepted: June 07, 2016

10.3928/23258160-20160808-05

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