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ISSN : 1229-6457(Print)
ISSN : 2466-040X(Online)
The Korean Journal of Vision Science Vol.23 No.3 pp.237-245
DOI : https://doi.org/10.17337/JMBI.2021.23.3.237

Binocular Visual Function in Patients with Normal Tension Glaucoma

Jung-Un Jang1), Joo-Hyung Choi2), Yoon-Jung Choy1)*, Koon-Ja Lee1)*
1)Dept. of Optometry, Eulji University, Professor, Seongnam
2)Dept. of Optometry, Graduate School of Public Health, Eulji University, Students, Daejeon
* Address reprint requests to Koon-Ja Lee (https://orcid.org/0000-0001-5867-5615) Dept. of Optometry, Eulji University, Seongnam
TEL: +82-31-740-7182, E-mail: kjl@eulji.ac.kr
June 1, 2021 September 23, 2021 September 27, 2021

Abstract


Purpose : This study aims to describe the binocular visual function alterations in patients with normal tension glaucoma (NTG).



Methods : Of the patients who went to the ophthalmologist and were diagnosed, a total of 67 subjects of which 41 were classified as NTG, 26 non-glaucoma patients (control group) were participated. Standard visual field test, intra ocular pressure (IOP) measurement and retinal nerve fiber layer (RNFL) obsevation were performed. Also examined with binocular tests consisting of the measurement of phoria angles, near point of convergence (NPC), stereo acuity according to Titmus and TNO stereo tests. All measurements among groups were statistically compared with the SPSS 22.0 and ROC curves were plotted to describe the screening ability of binocular and stereopsis values.



Results : NTG subjects showed decreased RNFL and visual field index. In far and near vision, NTG subjects were worse compared to in the control group except for fusional reserve. In Titmus test, NTG subjects exhibited stereo acuity of 102.36±14.40" whereas control group exhibited 44.61±1.85". In TNO test showed 231.97±30.96" for the NTG and 89.42±12.02" for the control group. The area under ROC for Titmus and TNO stereo test were 0.797 and 0.807. The sensitivity, specificity of Titmus stereo test were 0.737 and 0.731, and those of TNO stereo test were 0.500 and 0.115.



Conclusion : Titmus stereo acuity could be used as the gold standard for screening tools for NTG.


Binocular visual function , Normal tension glaucoma , Stereo acuity , Titmus stereo test

정상 안압 녹내장 환자의 양안 시기능

장 정운1), 최 주형2), 최 윤정1)*, 이 군자1)*
1)을지대학교 안경광학과, 교수, 성남
2)을지대학교 보건대학원 안경광학과, 학생, 대전

    Ⅰ. Introduction

    Normal tention glaucoma (NTG) is a progressive optic neuropathy with IOP within the normal range (≤21 mmHg). The main clinical features include normal angles on gonioscopy, cupping of the optic nerve, and visual field loss correlated with cupping that shows the progressive damage of the optic nerve.1-3) Glaucoma affects more than 66 million people and is the second leading cause of visual loss world wide.4,5) Recent studies from Japan, Mongolia, India, Singapore, Thailand, China, Singapore and Africa have reported the prevalence of NTG.6-11) Also, the prevalence of NTG is the most prevalent open-angle glaucoma (POAG) subtype in Korea.12-15) Goldmann applanation tonometry, gonioscopy, stereoscopic biomicroscopy of the optic nerve head, optical coherence tomography and Humphrey field analyzer are the main tools of investigation for diagnosis of NTG.16) However, the diagnosis and management of NTG have significantly difficulties in clinical practice that over half of NTG patients have without treatment and more difficult to detect changes in visual field damage even though undergoing treatment. The detecting progression and determining the rate of deterioration are more important in the management of NTG than other glaucoma. In the case of patients with glaucoma including NTG with visual field impairments, it has expected that the binocular abnormalities including stero acuity would be detected and reported stereo acuity, the higher grade of binocular function was affected in glaucoma patients.17-20) It has been reported that an association of decreased stereo acuity and other functional tests like visual acuity, contrast sensitivity and reduced quality of life scores with visual field defects in glaucoma subjects.21,22) Because the upper visual field defect occurs in NTG patients are different in compared to the POAG, the binocular vision and stereo acuity can be different in the known POAG. The Receiver operating characteristic (ROC) curve is a method to objectively evaluate the diagnostic ability of a diagnostic method. Areas under receiver operating characteristics (AUCs) is known as the criterion for measuring the discriminant force. According to Park et al,23) evaluation of the progression of diabetic retinopathy was confirmed by the waveform change of the electroretinography, and the clinical significance of the wave forms was evaluated by the ROC curve. As well reported that web-based validation had very high clinical, diagnostic, prognostic and therapeutic power confirmed by ROC curve.24) Also performed ROC curve to estimate the accuracy of prediction for the presence of glaucomatous damage by isolated-check visual evoked potential in early stage of POAG patients.25) Therefore, in this study, we assessed the binocular visual function including stereo acuity among NTG patients and determine the usefulness of the binocular test parameters using ROC curve.

    Ⅱ. Materials and Methods

    1. Subject

    Sixty-seven subjects were recruited from the eye clinic in the Hospital of the J in Bundang. Of the glaucoma patients who were diagnosed as NTG were 41 and 26 non-glaucoma patients (control group) were participated. The study was approved by the Research Ethics Committee of the Graduate School of Medicine and Faculty of Medicine at the University of Eulji (EU 2019-06). Written consent was given by the subjects for their information to be stored in the hospital database and used for research. Subjects with glaucoma diagnosed by the ophthalmologist. Among the glaucoma patients who had a cataracts and macular degenerative diseases, anomalies greater than 6.00 D, history of amblyopia, intraocular surgery, and patients with sympathetic and parasympathetic nerves were excluded. The control subjects were required to have no glaucoma with optic neuropathy and IOP was below the 21mmHg. NTG subjects were required to have progressive opticneuropathy that results in a characteristic optic nerve head cupping, retinal nerve fiber damage and functional visual field defects open anterior chamber angles are associated with IOP constantly below 21 mmHg.

    2. Eye examination

    The examination included the assessment of visual acuity and refractive error and binocular function test. IOP test was used to non-tonometer (NCT, CT-80, Topcon, Japan) and measured three times. Visual field testing was carried out monocularly using the Humphrey Field Analyzer (Humphrey Instruments, AII-750I, Carl Zeiss, Germany) SITA Fast 24–2 strategy (hereafter referred to as HVF) as well as binocularly using Humphrey Field Analyzer with Esterman strategy (hereafter referred to as HEVF) in a random order on the same day. Test reliability was not included with the help of Humphrey criteria such as false positive ( >33%) and false-negative error ( >33%). Mean deviation (MD) was used to aid analysis of the results. Thickness measured used to optical coherence tomography (OCY, 4000, Carl Zeiss, Germany) with Disc Cube 200×200 mode.

    Binocular visual functions (i) NPC: NPC was evaluated with the standard push-up technique using a fixation stick (Bernell, Mishawaka, IN, USA). The patient was seated and requested to follow the approaching target. For the test, the ruler was held at the center of patient's forehead at the level of the brow and the target was moved toward the patient at 15°. The break value was measured as the average of three measurements in which the examiner detects one eye deviation or the patient announced diplopia. The recovery value was measured as the average of three measurements in which the examiner detects that the patient's eyes appear to be realigned or the patient announced single vision.

    • (ii) Distance and near horizontal heterophoria: to assess the quality of general binocular vision system, the tests were performed with the best refractive correction in place. The cover test and cover-uncovered test was used to determine distance and near phoria with prism bar.

    • (iii) Distance and near fusional vergence: distance and near positive and negative fusional vergence were measured using a phoropter (HDR-7000, Huvitz, Anyang, Korea) and near chart. For distance positive and negative fusional vergence, Risley rotary prisms were used and approximately equal amounts of prism were slowly added in front of each eye at a constant velocity (2Δ/s) until the patient reported horizontal diplopia (break point). The amounts of prism were then reduced until the patient reported that the images were fused again (recovery point). For near negative fusional vergence, Risle prisms on both eyes with the zero in the vertical position was placed and equal amounts of base-in prism were added at the same rate to both eyes. When the patient reported diplopia (break) the prism was reduced in the opposite direction until the patient reported a single image (recovery). The total amount of prism for the right eye and left eye for negative fusional reserve was recorded. For near positive fusional vergence, the same procedure as near negative fusional vergence except base-out prism was used.

    • (iv) Stereopsistest: the Titmus-fly stereotest (Stereo, Stereo OPI, USA) and the TNO stereotest (TNO, Lameris Tech., Netherlands). All the patients underwent a stereopsis test with their own glasses. There have been no clear definitions of normal stereopsis that stands for bifixation. Forty to 60 seconds of arc is usually accepted as normal stereopsis. Also, the screening test used ROC curve were decided to screening-off point limits the specificity to more than 95% and provides the best sensitivity.

    3. Statistical analysis

    Completed examination data were collected and analyzed. Analysis was conducted, Kruskal-Wallis, Mann-Whitney, Pearson correlation using SPSS (Version 22.0 for Windows, SPSS Inc., Chicago, IL, USA). ROC curves were plotted to describe the screening ability of binocular and stereopsis values to differentiate between different glaucoma stages. Validation of the best cut-off was performed over 95%. The AUC values were considered as a measure to quantify the relative performance.

    Ⅲ. Results

    NTG subjects showed decreased RNFL and visual field index, but, no statistically significant differences were found in spectacle corrected visual acuity, age, spherical equivalent or gender of the 2 studied groups (p<0.050). Also, visual field MD, index and RNFL (Table 1). For these variables differences were found between control group and NTG subjects.

    In far and near vision, NTG subjects were worse than the control group except fusional reserve. Among those, the NPC was a much higher in NTG subjects. Comparing the control group and NTG patients, significant differences was observed for the far, near phoria angles and far fusional reserve (p<0.050). Far fusional reserve and above near fusional reserve, was diminished in NTG patients against control group (Table 2).

    Table 3 shows distribution of the stereo acuity. Most of NTG patients showed reduced stereoacuity compared to control group. According to the Titmus test, NTG subjects exhibited stereo acuity of 102.36±14.40" whereas control group exhibited 44.61±1.85". As regards the TNO test showed 231.97±30.96" for the NTG and 89.42±12.02" for the control group. The stereo acuity of the NTG patients was statistically different to that of the control group.

    The area under the ROC curve in NTG patients with titumus test of 0.797 (95% CI lower bound 0.68; upper bound 0.90; p=0.001), the sensitivity and specificity were 0.737 and 0.731. TNO test among NTG patients had an area under the ROC curve of 0.807 (95% CI lower bound 0.69; upper bound 0.91; p=0.005), the sensitivity and specificity were 0.500 and 0.115. Near vision functional test among near phoria had an area under the ROC curve of 0.741 (95% CI lower bound 0.61; upper bound 0.86; p<0.050), the sensitivity and specificity were 0.684 and 0.731. Near point convergence had an area under the ROC curve of 0.831 (95% CI lower bound 0.72; upper bound 0.93; p=0.007), the sensitivity and specificity were 0.711 and 0.231 (Fig. 1.).

    Ⅳ. Discussion and Conclusions

    This study was to assess the binocular function include stereo acuity was performed NTG patients. We also studied the determined stereo acuity between control group and NTG. Several studies have evaluated the binocular function and glaucoma.17-22) And, the NPC of glaucoma presented over the normal value and statistically different to the values of the glaucoma and control subjects.26) In our study, NPC was much higher in the NTG patients. Also, previous studies reported that binocular vision is the ability to integrate visual stimuli reaching each eye into a single perception. This requires the formation of similar and good optical quality images in each retina as well as sensory fusion or simultaneous perception of both images and precise motor coordination of both eyes. The peripheral visual field depression which is typical symptom in the glaucoma patients could cause a weakening of fusion vergences with the diminished overall convergence capacity and the importance of the unequal stimulation of the peripheral retina for the production of fusion vergences.27,28) This study, far and near fusional reserve decreased in the NTG patients. It is considered that decreased visual field sensitivity of the NTG patients, which affects the near and far fusional reserve. In addition, these patients would require greater positive fusion demand due to be more exophoric in near vision. In what concern stero acuity, significant differences found when comparing the study groups both Titums and the TNO stereo test. Bassi et al, found statistically significant differences in stereo acuity between the glaucoma group and the other group.17) In this event, stereo acuity reduction would be related to the MD campimetric values. In a subsequent study, observed that stereoscopic acuity of glaucoma subjects 305.08" and of hypertensive subjects 118.2" differed statistically from those of control subjects 16.8".18) Also, previous study that explored stereopsis with the Frisby test and also found stereo acuity differences between glaucoma subjects 148.1" and ocular hypertense subjects 144.1" when compared to normal subjects 26.6".29) However, author does not specify the average campimetric MD of each group. In this study, stereo acuity of NTG patients and control group was statistically significant differences, suggesting that an early disruption of binocular vision could occur in glaucoma due to greater susceptibility of neuronal circuits which control the perception of disparity. El-Gohary et al. found that stereoscopic equities differed in over 200" and who worked with two study groups between glaucoma and control subjects, found that the former exhibited a mean stereo acuity of 55" whereas the control group had 40".36.26) The visual acuities of both groups did not exhibit statistically significant differences. In this study performed the area under the ROC curve also. ROC curve in NTG patients with Titumus stero test 0.797 (95% CI lower bound 0.68; upper bound 0.90; p=0.001), the sensitivity and specificity were 0.737 and 0.731. TNO test among NTG patients had an area under the ROC curve of 0.807 (95% CI lower bound 0.69; upper bound 0.91; p=0.005), the sensitivity and specificity were 0.500 and 0.115. In term of prescribing for the area under ROC was 0.5 (95% CI – 0.292, 0.714) for both Frisby and Titmus stereo test for screening an inter ocular difference of≥0.1 logMAR.30) Also, the frequencies reported were 74, 68 and 62% respectively.31) Ohlsson et al. reported the sensitivities of various stereo tests for detection of amblyopia as 36% for Randot E, 38% for Titmus, and 46% for TNO. Moreover, Titmus stereo test sensitivity 75% and specificity 13%, frisby stereo test sensitivity and specificity were 75% and 27%.32) The screening qualities of stereo acuity showed inconsistent results as reported in literature. Our conclusions are on the stereopsis for the NTG patients are similar to the findings of previous studies. On the basis of this assumption, stereoacuity reduction would be fundamentally related to campimetric deterioration. This study provides double stereo acuity measurement due to the utilization of two different tests. The stereo acuity values provided by the Titmus test were better than those delivered by TNO for each study group. This could be due to the different sensory nature of the visible disparity in each test responds to a different mode of binocular disruption.20) Stereo acuity in patients with glaucoma has been reported in this study and previous studies, and stereo acuity is significantly worse in patients with glaucoma than in normal subjects. The decrease in stereo acuity in patients with glaucoma has been reported to occur due to the relative delay in the input of visual information in the cerebral cortex and it may also occur in early glaucoma where visual field defects are not evident. Though the Titmus stereo acuity tests could be used as a screening tool for the NTG, however it can not be used as a screening tool to detect the inter-ocular difference.

    Figure

    KJVS-23-3-237_F1.gif

    Binocular visual functions of ROC curve. (a): ROC curve the stereo acuity between control and normal tension glaucoma, (b): ROC curve the near phoria and near point convergence.

    Table

    Baseline data of study population

    Discriminating of binocular vision variables between control and normal tension glaucoma

    Stereoacuity between control and normal tension glaucoma

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