International Journal of Retina (IJRETINA) 2025.
Volume 8.
Number 1.
P-ISSN.
E-ISSN.
Differences of Retinal Nerve Fiber Layer and Ganglion Cell Layer-Inner Plexiform Layer Thickness in Patients without Diabetes Mellitus, with Diabetes Mellitus Type 2 without Diabetic Retinopathy and with Diabetic Retinopathy Ari Suryathi NM 1,2.
Andayani A 1,2.
Sukmawati NLP 1,2.
Pantjawati NLD4.
Yuliawati P 1,2.
Juliari IGAM 1,2.
Widiana IGR3 Department of Ophthalmology.
Medical Faculty of Udayana University Prof.
Dr.
Ngoerah Hospital Medical Faculty of Udayana University Department of Ophthalmology.
Bali Mandara Eye Hospital Abstract Introduction: Prevention of Diabetic Retinopathy (DR) require an examination method that can identify earliest damage before clinical symptoms observed.
This study aimed to determine the novel and objective way to detect those damage through RNFL and GCL-IPL thickness.
Methods: This analytical cross sectional study research conducted at the eye polyclinic and the Diabetic Center of IGNG Ngoerah Hospital.
Denpasar.
This study comparing the difference in thickness of RNFL and GCL-IPL in patients without DM, with Type 2 DM without DR and with DR in average and each quadrant thickness through Kruskal Wallis and One Way Anova test.
Results: The sample was 59 people which then divided into three groups, namely 20 samples in the group without DM, 19 samples in the DM group without DR and 20 samples with DR.
The samples were then examined for RNFL and GCL-IPL and the results were compared between groups.
The mean age of the subjects were 58.
80A9.
65 years old.
In the RNFL measurement, it was found that there were differences in values between groups in all quadrants except the temporal quadrant .
=0.
After covariate analysis by variables of age.
HbA1c, blood pressure, visual acuity.
IOP and axial length, the results change with the nasal and inferior quadrants as the only found significant.
In the GCL-IPL analysis there were significant differences between groups, especially in the superotemporal, temporal and inferotemporal quadrants .
<0.
These results remained after being controlled by covariate analysis.
Conclusion: This study proved a neurodegeneration process that occured focally in certain areas that can be detected through the RNFL and GCL-IPL measurement modalities.
These examinations were expected to be useful in terms of screening both primary and secondary in patients with type 2 DM.
Keywords: Diabetes Mellitus Type 2.
Diabetic Retinopathy.
Retinal Nerve Fiber Layer.
Ganglion Cell LayerInner Plexiform Layer Cite This Article: SUKMAWATI.
Nurindah et al.
Differences of Retinal Nerve Fiber Layer and Ganglion Cell Layer-Inner Plexiform Layer Thickness in Patients without Diabetes Mellitus, with Diabetes Mellitus Type 2 without Diabetic Retinopathy and with Diabetic Retinopathy.
International Journal of Retina, [S.
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Available <https://w.
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Date accessed: 04 mar.
doi: https://doi.
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35479/ijretina.
Published by: INAVRS https://w.
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diabetic retinopathy patients and in the control
INTRODUCTION
Correspondence to:
Nurindah sukmawati.
Universitas Udayana Bali.
Indonesia, nlp@gmail.
Diabetic retinopathy (DR) .
But those studies is known to only display is a complication of type 2 the RNFL thickness parameter as a single parameter.
especially at an advanced .
Diabetic retinopathy was the 6th leading cause of moderate to severe visual impairment in the global population in 2015.
Global meta-analysis in the United States.
Australia.
Europe, and Asia reported that 1 in 3 patients with DM had diabetic retinopathy, and 1 in 10 .
2%) patients had visionthreatening DR, namely proliferative type DR or diabetic macular edema.
DM sufferers in the world are estimated to increase to 191 million people and around 56.
3 million will experience DR in 2030 without adequate prevention.
There are also other parameters that can indicate the presence of neurodegeneration in the retina, such as the thickness of the GCL-IPL layer and GCC Booroah et al .
showed that the mean Ganglion Cell Layer-Inner Plexiform Layer (GCL-IPL) in patients without diabetic retinopathy was found to be thinner than the control group.
Ganglion Cell Complex (GCC) is a complex consisting of RNFL.
GCL and IPL.
This layer previously had clinical value in the early detection of retinal damage associated with glaucoma.
Ganglion Cell Complex represents the loss of dendrites characterized by depletion of IPL, while ganglion cell bodies present in the GCL and nerve axons that can be assessed from the Prevention of diabetic retinopathy requires an thickness of the NFL.
examination method that can identify damage as early as possible before clinical symptoms can be Diabetic retinopathy primarily caused by microvascular damage due to the disintegration of the blood-retinal barrier, resulting in impaired neurovascular interaction.
The retinal nerve fiber layer (RNFL) is the main component of the inner retinal layer.
Changes in the RNFL are assumed to detect neurodegeneration processes in patients with DM.
The differences between RNFL.
GCL and IPL can Spectral Domain-Optical Coherence Tomography (SD-OCT).
As a complement to previous studies, this study not only displays data on the thickness of the RNFL but also other parameters that also show the degeneration process, such as the thickness of GCL-IPL in various quadrants so that the conclusions obtained will be more This study aimed to compare differences in RNFL thickness and GCL-IPL thickness in patients RNFL without DM, patients with DM without DR and in retinopathy has shown mixed results in previous patients with diabetic retinopathy using the SD-OCT Research by Li, et al.
, showed that RNFL It is expected that the results of this study can correlated with vascular density in the optic nerve.
contribute to education, early detection and clinical The study showed a significant relationship between consideration of providing neuroprotective therapy RNFL thickness and optic nerve vascular density in before irreversible microvascular damage occurs.
DM patients without and with diabetic retinopathy.
The study conducted by El Hifnawi, et al.
, showed that there was no significant difference between the thickness of each RNFL quadrant in the group of healthy individuals and the group with NPDR.
Another study conducted showed that there was no significant difference between RNFL thickness in METHODS This cross-sectional Data collection conducted prospectively.
Sampling was carried out consecutively using primary data.
The study was conducted at the Eye Polyclinic and the Diabetic Center Polyclinic of the IGNG Ngoerah Hospital Denpasar by recording Published by: INAVRS https://w.
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patient data for ONH-OCT (RNFL dat.
and macular have eye pressure >21 mmHg measured by OCT (GCL IPL dat.
in June 2021-December 2021.
Goldmann applanation, subjects whose axial length The target population was divided into three groups, namely for the group without diabetes, the target population was patients without diabetes For the group with diabetes without diabetic retinopathy, the target population is patients with type 2 diabetes.
The group without type 2 diabetes mellitus was obtained from ophthalmology polyclinic patients who underwent medical check-ups or who had only anterior segment abnormalities such as mild refractive errors of the eyeball is beyond the normal limit, i.
length >25 mm or <23mm measured by noncontact optical biometry, history of congenital optic neuropathy, history of ocular trauma, papillary OCT results with signal strength <6/10, a history of previous eye surgery and history of previous active intraocular infection.
The DM group inclusion criteria only including the type 2 DM.
The DR subjects were subject that confirmed by fundus photography by 2 senior consultants (AA and AS).
or mild cataracts (Peng, et al.
, 2.
The group with The null hypoteses was there was no differences diabetes mellitus without diabetic retinopathy was between the average or each quadrant between the taken from the Diabetic Center Polyclinic of IGNG three group.
Ngoerah Hospital.
The retinopathy was obtained from diabetic retinopathy patients who came to Vitreoretinal division of Ophthalmology Polyclinic and patients from the Diabetic Center who on examination found diabetic All samples was taken consecutively based on minimum sample requirement.
The inclusion criteria for non DM group was subjects aged 40-70 years and without a history of any type of diabetes, subjects can be from opthalmology polyclinic patients who are checked for medical check-up, patients with refractive errors not less than Sph -3D and not greater than 3D, or cataract patients with minimal lens opacities with maximum lens opacities NO4NC4 or P4 if there is posterior subcapsular opacification (LOCS criteri.
and willing to be the subject and have a complete eye examination including pupil dilation.
ONH and macular OCT.
The exclusion criteria was subjects with glaucoma All the data was calculated using Anova test if normally distributed and Kruskal-wallis if not normally distributed.
Covariate analysis calculated with covariates as followed:
Age.
HbA1c, blood pressure, visual acuity.
IOP, axial length because those variable may contribute as a potential The p value is declared significant if p <0.
Calculation was done using SPSS 15.
RESULTS
The sample of this study consisted of 59 people population, namely all patients who came to the Eye Polyclinic and Diabetic Center at Sanglah General Hospital.
Denpasar, who met the inclusion and exclusion criteria.
The sample was divided into three groups: 20 patients without Diabetes Mellitus, 19 retinopathy, and 20 patients in the group with diabetic retinopathy (Table 5.
No missing data in this report.
or have a history of glaucoma or have a family with glaucoma, with Type 1 Diabetes Mellitus, subjects Published by: INAVRS https://w.
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Table 5.
Characteristics of the Research Sample Without DM
DMT 2 without DR With DR n:20 n:19 n: 20
55,57A7,72
62,37A10,99
58,45A9,37
Male
,4%)
,5%)
,1%)
Female 13 .
,1%) 9 .
,0%) 14 .
,9%) 11 .
,3%) 9 .
,1%) 8 .
,6%) Variable Avg Age .
(MeanASD) Sex, n (%) Domicile, n (%) Denpasar
Outside Denpasar
,0%)
,3%)
,7%)
Laterality, n (%) Right eye (OD) 9 .
,1%) 11 .
,3%) 8 .
,6%) Left Eye (OS) 11 .
,5%) 8 .
,8%) 12 .
,7%) 6 .
90,50 .
91,00 .
90,00 .
Axial Length .
(Median(IQR)) 24,5 .
23,9 .
24,2 .
Visual Acuity .
ogMAR) (Median (IQR)) 00 .
0,20 .
0,55 .
IOP (MeanASD) 13,85A2,47 12,37A2,89 12,70A2,99 Central Macular Thickness (Median(IQR)) 255,5 .
244,0 .
257,0 .
HbA1c (Median(IQR)) 4,35 .
8,9 .
8,65 .
Duration of Diabetes .
(Median(IQR)) Blood Pressure (MAP) .
(Median(IQR)) Measurement of the difference in OCT RNFL We also try to assess the influence of potential values in each quadrant is summarized in table 5.
bias through covariate analysis.
After covariate The distribution of RNFL data on all means was not analysis with assumed confounding variables, such normally distributed .
value> 0.
05 using Shapiro- as age.
HbA1c, blood pressure, visual acuity.
IOP.
Wilk analysi.
The results of bivariate analysis in axial length, it was found that the quadrants that had more than two groups were not normally distributed significant differences were the nasal and inferior with the Kruskal-Wallis Test showing that in all This shows that there are confounding variables that have an influence on the thickness of between groups, both in the inferior, superior, nasal the RNFL.
Variables that significantly proved to be and mean quadrants, except for the RNFL temporal influential included: age .
=0.
and axial length In the calculation of the temporal .
=0.
Other variables, namely HbA1c, blood quadrant RNFL, there was no significant difference pressure, vision and IOP, did not prove to have an with a value of p = 0.
effect on RNFL thickness in the three groups .
>0.
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Table 5.
Differences in Retinal Nerve Fiber Layer (RNFL) values between groups RNFL (AA.
(Median(IQR) Without DM DMT 2 without DR With DR Bivariate p Covariate p Inferior 155,50 .
138,00 .
128,50 .
0,000
0,021
Superior 122,0 .
98,00 .
89,00 .
0,001
0,202
Nasal 121,00 .
106,00 .
77,50 .
0,041
0,045
Temporal 93,00 .
83,00 .
92,50 .
0,518 0,297 Rerata (Averag.
122,37 .
105,5 .
96,37 .
0,000 0,121 *P-value was calculated using the Kruskal Wallis Test, p-value was significant if p<0.
05 **Covariate analysis results (ANCOVA) with covariates: Age.
HbA1c, blood pressure, visual acuity.
IOP, axial length.
The p value is declared significant if p <0.
All data in the table is not normally distributed.
The distribution of GCL-IPL data for all means was not normally distributed .
value> 0.
05 by Shapiro-Wilk analysi.
except for the average GCL-IPL value .
<0.
Bivariate analysis with One Way ANOVA was used for normally distributed data, while the Kruskal-Wallis Test was used for non-normally distributed In the statistical results, it was found that there was a decrease in each quadrant, but what showed significant results was from the temporal quadrant, namely inferotemporal, superotemporal, temporal and the mean GCL-IPL value.
The other quadrants, although showing decreasing values according to the presence or absence of diabetic retinopathy, did not show statistically significant differences .
value> 0.
These results remained the same even after covariate analysis was performed.
This shows that the confounding variables, namely age.
HbA1c, blood pressure, visual acuity.
IOP, axial length, did not prove to have an effect on the thickness of GCL-IPL .
>0.
Table 5.
Differences in Ganglion Cell Layer-Inner Plexiform Layer (GCL-IPL) values between groups GCL-IPL-(AA.
Without DM
DMT 2
with DR Bivariate p Covariate p (Median(IQR) without DR value*** Inferior 109,00 .
108,00 .
108,00 .
0,677*
0,158
Inferonasal 119,00 .
114,00 .
109,50 .
0,796* 0,200 Inferotemporal 109,50 .
87,00 .
0,000* 0,000 Superior 113,00 .
110,00 .
108,50 .
0,380*
0,500
Superonasal 123,50 .
111,00 .
108,0 .
0,169* 0,253 Superotemporal 115,00 .
96,00 .
0,000* 0,009 Nasal 122,25 .
112,00 .
110,25 .
0,114*
0,289
Temporal 171,00 .
113,50 .
103,25 .
0,000* 0,000 Rerata (Averag.
146,96A17,8 125,40A18,6 109,28A21 0,000** 0,000 *Kruskal Wallis Test results.
The p value is considered significant if p <0.
05 ** One Way Anova Test results.
The p value was declared significant if p <0.
05 *** Results of covariate analysis (ANCOVA) with covariates: Age.
HbA1c, blood pressure, vision.
IOP, axial The p value is declared significant if p <0.
All data in the table is not normally distributed except the average GCL-IPL.
DISCUSSION
the eyes of patients with type 2 DM without DR This study showed that there was a statistically which were seen clinically, especially in the area close significant decrease in the average .
RNFL to the optic disc.
Other studies that between groups.
Several studies conducted in the compared control patients with patients with type 2 DM group without and with mild NPDR diabetic retinopathy also showed a significant showed similar results.
The results of those studies reduction in the mean RNFL.
,12,.
emphasized the presence of neurogenic changes in Published by: INAVRS https://w.
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In this study, in addition to the difference in performed on subjects who have a low axial length mean between groups, the temporal quadrant is the (<23m.
, the ganglion cell density will be increases only quadrant that is not showing significant and results in thicker RNFL measurements.
This study is in line with previous metaanalysis studies which showed that the temporal quadrant of the RNFL did not experience the same thinning as other quadrants.
This is related to capillary perfusion and the highest flux index in the temporal quadrant including superotemporal and inferotemporal as evidenced by previous OCT Angiography examinations study performed in the .
The results of the covariate analysis also showed that HbA1c had no effect on differences in the results of RNFL thickness.
These results indicate that the neurodegeneration that occurs is more conducive to vascular causes than the effect of metabolic control.
The study conducted by Nor-Sharina, et al.
suggested using Hemoglobin Advanced Glycation End-products (Hb-AGE) as a more stable metabolic parameter compared to HbA1c.
Other parameters can also be used such as GDP or GDS with similar This study also shows that the condition of type Chihara, et al.
also showed that HbA1c 2 DM can affect neurons, especially in the Optic was not related to the degree of diabetic Nerve Head (ONH) and this condition can be The study also assumes that there are observed by OCT examination of the ONH.
After other pathogenesis such as ischemia which can controlling for confounding variables using covariate underlie the decrease in the thickness of the analysis, such as age.
HbA1c, blood pressure, vision.
RNFL.
IOP, axial length, there was a thinning that was still found to be significant in the nasal and inferior This proved that there is a confounding variable effect on the thickness of the RNFL.
Through the covariate analysis, we found that confounding variables that may influence the result was age and axial length.
Previously it was known that an increase in age is associated with a decrease in the thickness of RNFL and GCL-IPL, which is around 0.
26% or 54 AAm per year .
and reaches 0.
per year at the age of over 75 years.
This is due to a decrease in vascular density and structure related to aging which increases the process of In line with the this study, a meta-analysis conducted by Chen, et al.
also found thinning in the superior, inferior and nasal areas associated with increased of retinal medial layer thickness in the choroidal vessels.
,15,.
Shahidi, et al.
and Shi, et al.
showed that the inferior quadrant showed significant depletion compared to normal .
These results are expected to be the basis for the development of screening of patients with preclinical diabetic retinopathy which is convincingly towards vascular factors rather than metabolic factors.
apoptosis in ganglion cells.
Long axial length In contrast to the studies previously described, in previous studies was associated with a decrease in other studies showed no significant thinning in the ganglion cell density.
So that the RNFL thickness inferior quadrant.
Study by Sugimoto, et al.
measurement will show thinner results if it is done .
showed that the superior quadrant has on subjects with a long axial length .
ore than 25 This could be related to the higher scan .
,15,.
Other studies also showed that distance in patients with high axial length and the RNFL values in patients with type 2 DM were not presence of stretching of the Bruch's Membrane significantly different compared to controls, but this Opening (BMO).
Likewise, if the measurement is study did not include samples with diabetic Published by: INAVRS https://w.
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retinopathy and did not perform a standard fundus photo examination.
These results remained the same after controlling for confounding variables such as The average value of the GCL in this study showed a significant difference between the three These results are similar to a study conducted by Van Dijk, et al.
, .
, which found a thinner GCL layer in the pericentral area of the macula in patients with mild NPDR compared to patients without diabetes.
Meyer-Rysenberg, et al.
showed a decrease in the number of midget cells and parasol cells in the GCL-IPL layer that occurred in patients with Type 2 DM.
Another study also showed that the average GCL-IPL thickness was lower in patients with diabetes compared to control patients, although there was no significant difference in mean RNFL.
The result age.
HbA1c, visual acuity.
CMT and axial length.
These results may indicate that the confounding variable has no effect on the GCL-IPL thickness results including the glycemic control variable or HbA1c.
Similar to the results of RNFL analysis, the factor that has a greater role in the difference in GCLIPL thickness is the vascular factor.
This is supported by research by Byeon, et al.
who showed an expansion of the FAZ (Foveal Avascular Zon.
area seen on OCT Angiography associated with damage to the GCL-IPL layer in the fovea.
The expansion of the FAZ area indicates a macular ischemic condition in patients with diabetic retinopathy due to loss of vascular blood supply.
from this study and as supported by previous There are three vascular networks that supply studies, shows that there is damage to neurons on the macula, namely the Superficial Capillary Plexus the macula that can be objectively measured (SCP).
Deep Capillary Plexus (DCP) and the through the thickness of the GCL-IPL.
According to several studies, these results are caused by the superficial capillary plexus (SCP) supplies the presence of hyperglycemia which causes an increase superficial retinal layer area from the inner plexiform in the release of VEGF.
NO, glutamate, inflammatory layer down to 15.
6 m below the inner plexiform cytokines and ROS (Reactive Oxygen Specie.
This layer (IPL), and the DCP supplies the underlying layer.
process can cause retinal ganglion cell apoptosis The Choriocapillaris (CC) layer supplies the bruch through various mechanisms such as BRB disruption, membrane area to 10.
4 m below it.
Vascular neuronal excitotoxicity, and increased intracellular density and capillary flux in SCP were found to be calcium accumulation.
lower in patients with microvascular disorders Although little is known about optic nerve dysfunction in patients with diabetes mellitus, some postulate that the diabetic condition affects the anterograde and retrograde transport of large and medium sized ganglion cell axons even though there is no quantitative or morphological abnormality of these cells.
(CC
The including diabetes.
Macular vascular density was found to be lower in patients with diabetes, but the association was found to be significant only in the temporal area.
The low density of blood vessels in the temporal area in diabetic patients is assumed to occur due to early capillary dropout which occurs before there are clinically identifiable signs of diabetic retinopathy.
Another study also found This study not only showed that there is a similar capillary dropout using other imaging difference in the average GCL-IPL between groups, .
Apart from the dropout, this but also shows that there is depletion that occurs in decrease in density is also caused by an increase in certain quadrants, namely the temporal quadrant the fovea avascular zone in patients with diabetes.
In a study conducted by Attalah, et al.
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the presence of the Avascular Fovea Zone (FAZ), levels, namely 5%, 2% and 1%, compared with both superficial and deep retinal plexus, is associated patients without DM.
This defect was found to be with a decrease in fovea thickness.
In patients with more likely to occur symmetrically and tend to have a diffuse pattern.
enlarged FAZ areas are mainly found in the superficial plexus, so it is assumed that the process of decreasing foveal thickness is influenced by the superficial plexus layer.
However, several other studies have shown different results.
The study conducted by Araszkiewicz, et al.
showed different results, namely in patients with diabetes mellitus without diabetic retinopathy, the GCL was thicker than the control group without diabetes mellitus, especially in the superior and inferior .
,47,.
These results are assumed to be mechanisms that cannot be explained.
In another study by Hegazy, et al.
, .
, the volume of GCL-IPL differed significantly in mean, superior and inferior values.
This suggests that GCLIPL depletion in patients with diabetes shows a more focal thinning pattern compared to a diffuse thinning pattern.
Not all studies show similar results with this study, the study by Te, et al.
showed that there was no significant difference between patients with type 2 DM without diabetic retinopathy and those with mild NPDR using the Short Wavelength Automated Perimetry (SWAP) device .
This study shows that DMT 2 is different from DMT 1 which is a disorder caused by a single disorder, namely insulin deficiency while DMT2 is a multifactorial process with various pathogenesis and manifestations.
Pathogenesis pathways that are most often studied include metabolic factors and vascular factors.
In this study, we emphasize the dominant link between neurodegeneration and vascular factors compared to metabolic factors.
There are some of the weaknesses of this study.
The method used is cross-sectional, making it difficult to determine the causal relationship Sahin, et al.
showed that there was a neurodegenerative changes.
The research does not negative correlation between HbA1c and RNFL mean reflect differences based on time, so it is necessary and assumed that RNFL depletion could be due to to carry out a longer prospective study so that it can increased atherosclerosis in patients with type 2 DM be determined whether there is a decrease in the associated with poor glycemic control.
thickness density of RNFL and GCL-IPL.
The study did Although data recorded were not assessing ganglion cell function, the results of this study were supported by several previous studies which indicated functional defects, such as visual field not distinguish between non-proliferative and proliferative diabetic retinopathy, so this study should be continued to obtain results that include subgroup analysis.
abnormalities, contrast sensitivity and color as We are further suggest further research is evidenced by a decrease in the value of the Ishihara needed regarding the analysis of subgroups of panel.
Lanthony 15-hue desaturated panel, and patients with diabetic retinopathy with various FarnsworthAeMunsell 100-hue test in patients with degrees, namely the nonproliferative type and the type 2 DM.
Another study using Frequency proliferative type or involving diabetic retinopathy Doubling Technology (FDT) showed that patients patients after laser procedures or intravitreal with T2DM without diabetic retinopathy were more Further research development can be likely to have Ou10 subfield defects at all sensitivity carried out by examining the presence of visual field Published by: INAVRS https://w.
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defects, contrast and color vision in patients with preclinical diabetic retinopathy.
The existence of this paper opens the opportunities for conducting various similar studies in various scientific disciplines other than the field of the eye as a target organ, such as the fields of nephrology, cardiology, and the central and peripheral nervous system.
Udayana University VII.
14/LT/2021.
All 2808/UN agreed to informed consent before participate.
Consent for Publication The Publisher has the Author's permission to publish the relevant Contribution CONCLUSION There are differences in RNFL thickness in all quadrants between groups except the temporal The quadrants that were most significantly Conflicts of Interests:
The authors declare no competing interests thinned were the nasal and inferior quadrants.
There Funding were significant differences in GCL-IPL thickness No funding or grant support between groups in the superotemporal, temporal and inferotemporal quadrants.
RNFL and GCL-IPL examinations then can be used in preventive.
Author contributions Conceptualization-AS,NS.
Methodology: RW,AS.
screening, diagnostic and prognostic efforts in Investigation,NS,DP.
diabetic patients even though clinical signs of NS,AS,AA,DP.
Writing-review and editing :PY,IJ,RW.
Supervision :AS,AA,DP,PY,IJ,RW.
Writing-original Preventive efforts can be made in the form of providing education about Diabetes Mellitus and the Acknowledgement possibility of thinning of the papillae and macula
None
which can be detected using the RNFL and GCL-IPL
Screening and diagnostics on RNFL
REFERENCES