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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 22  |  Issue : 1  |  Page : 34-41

Correlation of retinal nerve fiber layer and ganglion cell complex thickness with glycosylated hemoglobin in diabetic patients


Department of Ophthalmology, Faculty of Medicine, Beni-Suef University, Beni-Suef, Egypt

Date of Submission27-Jul-2020
Date of Decision10-Sep-2020
Date of Acceptance01-Nov-2020
Date of Web Publication24-Mar-2021

Correspondence Address:
MD Maria E.A Mikhail
Department of Ophthalmology, Faculty of Medicine, Beni-Suef University, Chejung House, Yonsei University, 03722, 50, Yonsei-ro, Seodaemun-gu, Seoul, South Korea. Zip/Postal Code: 03722
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/DJO.DJO_57_20

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  Abstract 

Aim The aim of this study was to correlate the retinal nerve fiber layer (RNFL) and ganglion cell complex (GCC) thickness with glycosylated hemoglobin (HbA1c) in diabetic patients.
Setting and design This is a comparative case series study that was conducted on 58 eyes of 30 diabetic patients attending the Outpatient Clinics of the Ophthalmology Department, Beni-Suef University Hospital, Beni-Suef, Egypt, between June and August 2019.
Patients and methods The 30 cases were divided into two equal groups: uncontrolled diabetic group (group 1), with HbA1c more than or equal to 7%, and controlled group (group 2), with HbA1c less than 7%. Both eyes in each patient were scanned using optical coherence tomography, ‘Optovue.’ Blood samples for HbA1c testing were collected as well.
Results There was a significant negative correlation between average, superior, inferior, and nasal RNFL quadrant thickness and HbA1c in group 1, which was found with HbA1c level more than 9%. In group 2, there was no statistically significant correlation of HbA1c and all RNFL parameters in both eyes. In addition, in group 1, there was a significant negative correlation of average, superior, and inferior GCC quadrant thickness and a positive correlation of focal loss volume with Hb1Ac level more than 9%. In group 2, the average and inferior GCC thickness showed a positive correlation with HbA1c. Furthermore, focal loss volume and global loss volume were negatively correlated with HbA1c.
Conclusion There was a statistically significant correlation between thinning of most of RNFL and GCC quadrants and uncontrolled HbA1c more than 9%.

Keywords: ganglion cell complex, glycosylated hemoglobin, retinal nerve fiber layer


How to cite this article:
Mikhail ME, Saif MYS, Mohammad SI. Correlation of retinal nerve fiber layer and ganglion cell complex thickness with glycosylated hemoglobin in diabetic patients. Delta J Ophthalmol 2021;22:34-41

How to cite this URL:
Mikhail ME, Saif MYS, Mohammad SI. Correlation of retinal nerve fiber layer and ganglion cell complex thickness with glycosylated hemoglobin in diabetic patients. Delta J Ophthalmol [serial online] 2021 [cited 2022 Aug 18];22:34-41. Available from: http://www.djo.eg.net/text.asp?2021/22/1/34/311894


  Introduction Top


Diabetes mellitus (DM) occurs when there is increased level of blood glucose [1]. The American Diabetes Association has recommended glycosylated hemoglobin ‘hemoglobin A1c’ (HbA1c) as a possible substitute to fasting blood glucose test. HbA1c correlates well with the long-term diabetic complications such as diabetic retinopathy (DR) [2]. DR is a progressive sight-threatening condition of retinal microvasculature and neurons [3].

It was believed that visual impairment in diabetic patients is due to retinal vascular lesions only. However, it is becoming increasingly clear that neuronal retinal cells are also affected by DR, leading to their dysfunction and degeneration [4], as DR causes impairment of neurovascular coupling, compromises endothelial-mural cell interactions, Muller cell gliosis, and immune cell activation [5]. Such anatomical and physiological changes of the diabetic retina highlight considering neural and vascular complications as potentially linked processes [6].

Studies aiming to investigate the possible influence of early retinopathy on the annual change of retinal nerve fiber layer (RNFL) thickness by using optical coherence tomography (OCT) have associated DM with thinning of the RNFL [7]. Significant ganglion cell complex (GCC) thinning in diabetics as well as RNFL thinning may predate retinal vasculopathy [8].

Spectral domain optical coherence tomography (RTVue-OCT) has proved to be a useful tool in early diagnosis of retinal neurodegeneration [9]. Thus, the present study hypothesis was developed. It aimed to detect whether there was a relationship between HbA1c level, as a diabetes monitor tool, and RFNL and GCC thinning, so that these neuroretinal changes could be employed as a predictive marker of the development of DR.


  Patients and methods Top


This comparative case series study was approved by the Faculty of Medicine Beni-Suef University Research Ethical Committee (FM-BSU REC). It was conducted according to the guidelines of the Declaration of Helsinki, International Conference of Harmonization (ICH) and United States Codes of Federal Regulations. It was registered under the Federal Wide Assurance (FWA) for the protection of Human Subjects (FWA#: FWA00015574, Expiry: 04/09/2023, Approval; FMBSUREC/16062019/Mikhail). All patients signed a written informed consent to participate in the study and for publication of data before being enrolled in the study. The consent was obtained from the participants after precise explanation of the nature, steps, and possible consequences of this study.

This study was conducted on a small sample size of 58 eyes of 30 diabetic patients on hypoglycemic medications for diabetes control. The studied patients were attending the Outpatient Clinics of the Ophthalmology Department, Beni-Suef University Hospital, Beni-Suef, Egypt, for checkup or follow-up of ocular diabetic changes between June and August 2019. All participants were Egyptians with age range of 40–70 years with or without DR. Included patients either did not have evidence of DR or mild nonproliferative DR, even in patients with long duration of DM. Any participant who had ocular or systemic disease that can affect the optic nerve, whether detected by history or by ocular examination such as glaucoma, hypertension, or diabetic papillopathy or who had poor quality scans was excluded from the study. In addition, patients with moderate or severe DR were also excluded from the study. Patients with mild diabetic macular edema (DME) were included. On the contrary, patients with moderate or severe DME were also excluded to avoid possible changes which can occur to the RNFL and GCC thickness.

All patients were subjected to a full medical and ophthalmic history taking, assessment of visual acuity and refraction, anterior segment examination by slit-lamp biomicroscopy and precise fundus examination by a 90-D lens.

RTVue optical coherence tomography

OCT images were obtained from both eyes of each patient by RTVue-OCT ‘Optovue’ (Optovue Inc., Fremont, California, USA). Images were obtained for RNFL average, four quadrant thicknesses, RNFL analysis maps, and Temporal-Superior-Nasal-Inferior-Temporal (TSNIT) analysis. GCC average, superior, and inferior thicknesses; focal loss volume (FLV); and global loss volume (GLV) were also obtained.

Glycosylated hemoglobin

In the same setting of OCT imaging, a blood sample was taken from every patient for HbA1c level analysis. The test was done under the standardization of the International Federation of Clinical Chemistry (IFCC) Reference Measurement Procedure (RMP) [10] using BTS Biosystem Analyzer and Glycohemoglobin HbA1-test human diagnostics.

HbA1c test provides evidence about an individual’s average blood glucose levels during the previous 2–3 months (half-life of the red blood cells) [2]. The diabetic cases were classified into two groups: uncontrolled with HbA1c more than or equal to 7% (group 1) and controlled with HbA1c less than 7% (group 2). This classification is according to the American Diabetes Association recommendations for the controlled HbA1c for adult diabetic patients to be less than 7% (53 mmol/mol). Diabetes Control and Complications Trial (DCCT) showed that better glycemic control was associated with significant decrease in the development and progression of microvascular retinopathy [11].

Statistical analysis

The collected data were categorized into demographic and medical data. They were then organized, tabulated, and statistically analyzed using SPSS software statistical computer package, version 22 (SPSS Inc., Chicago, Illinois, USA). For quantitative data, Kolmogorov–Smirnov test was performed as a test of normality. Age was normally distributed, and so the mean and SD were calculated, and independent t test was used to compare between the study groups. On the contrary, the other study parameters were not normally distributed, and so the median and range were calculated for them. The Mann–Whitney U test was used as a nonparametric test in comparing between study groups and in measuring the significance between two independent random variables. Moreover, for the qualitative data, it was presented as numbers and percentages, and χ2 was used as their test of significance. Pearson’s correlation coefficient was run to identify the relationship between HbA1c and the other study parameters such as best-corrected visual acuity and RNFL and GCC thickness. For interpretation of tests of significance, the results were considered significant at P value less than or equal to 0.05.


  Results Top


The study included 58 eyes of 30 diabetic patients on hypoglycemic medications for diabetic control. They included 16 (53.3%) males and 14 (46.7%) females. The mean age of the patients was 53.53±9.16 years in group 1 and 54.80±9.42 years in group 2. There was no statistically significant difference between the two groups regarding age or sex (P=0.712 and 0.143, respectively). There was also no statistically significant difference between the two groups in the duration of DM (P=0.367, [Table 1]).
Table 1 Duration of diabetes, level of glycosylated hemoglobin, and best-corrected visual acuity

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The study examined the right and left eyes separately to avoid any bias that may result from biological differences between the two eyes and also to prevent rejecting useful data.

Retinal nerve fiber layer thickness and its correlation with glycosylated hemoglobin in both groups

Group 1 had a statistically significantly lower average and temporal RNFL thickness in the right eye, (P=0.011 and 0.019, respectively) as well as lower inferior RNFL quadrant thickness in the right and left eyes (P=0.025 and 0.029, respectively) when compared with group 2. On the contrary, there was no statistically significant difference between the study groups regarding the other parameters of RNFL ([Table 2]).
Table 2 Difference between study groups regarding retinal nerve fiber layer thickness

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[Figure 1]a represents the variation in thickness of the five variables (average, superior, inferior, temporal, and nasal quadrants of RNFL) in relation to the variation in HbA1c level for the right eyes. All variables scored lower RNFL thickness values starting from HbA1c value=9.3 (>9%) in the majority of the study participants, which is a novel finding. The same finding was found in the left eyes as well ([Figure 1]b).
Figure 1 Changes in the retinal nerve fiber layer (RNFL) parameters (average, superior, inferior, temporal, and nasal) according to the change in glycosylated hemoglobin (HbA1c) level: (a) for the right eyes (RT), and (b) for the left eyes (LT).

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Regarding the correlation of HbA1c level and RNFL thickness, in group 1, there was a statistically significant negative correlation of HbA1c with average, superior, and inferior RNFL thicknesses in the right and left eyes (P=0.012, 0.019, and 0.003, respectively) and nasal RNFL quadrant thickness in the right eyes (P=0.001). On the contrary, within group 2, correlations of HbA1c and RNFL thickness in the different quadrants were insignificant (P=0.366, [Figure 2]).
Figure 2 Correlation of glycosylated hemoglobin (HbA1c) and retinal nerve fiber layer (RNFL) parameters in the right (RT) and left eyes (Lt) in both groups: (a) for group 1 (G1), and (b) for group 2 (G2).

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Ganglion cell complex thickness and its correlation with glycosylated hemoglobin in both groups

In group 1, a statistically significant lower average and inferior GCC thickness in the right eyes was found when compared with group 2 (P=0.002 and 0.006, respectively). Conversely, FLV in the left eyes and GLV in both eyes were statistically significantly higher in group 1 than in group 2 (P=0.001, 0.045, and 0.011, respectively). On the contrary, there were no statistically significant differences between the two study groups regarding the other parameters of GCC thickness ([Table 3]).
Table 3 Difference between study groups regarding ganglion cell complex thickness

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[Figure 3]a illustrates the GCC thickness (average, superior, and inferior quadrants of GCC) variations in relation to the variation in HbA1c level for the right eyes. As indicated, there was a global tendency of decreasing thickness of GCC variables starting from HbA1c value=9.3% (>9%) in the majority of the study participants, which is a new finding. The same observation was found in the left eyes as well ([Figure 3]c). In [Figure 3]b and d, the FLV and GLV showed a tendency to increase in both eyes. This increasing tendency started from HbA1c value of 9.3% (>9%).
Figure 3 Changes in ganglion cell complex (GCC) parameters [average, superior, and inferior GCC quadrants, focal loss volume (FLV), and global loss volume (GLV)] according to changes in glycosylated hemoglobin (HbA1c) level. Changes in the right eyes (RT) are shown in (a) average, superior and inferior GCC quadrants, and (b) FLV and GLV. Changes in the Left eyes are shown in (c) average, superior, and inferior GCC quadrants, and (d) FLV and GLV.

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For HbA1c correlation with GCC among group 1, there was a statistically significant negative correlation with average, superior, and inferior GCC in both eyes (P=0.001, 0.002, and 0.004, respectively). In contrast, there was a positive significant correlation between HbA1c and FLV in the right and left eyes (P=0.002). On the contrary, within group 2, there was a statistically significant positive correlation of HbA1c with average and inferior GCC in the left eyes (P=0.001 and 0.008, respectively) but still within normal limits ([Figure 4]). HbA1c was negatively correlated with FLV and GLV in right and left eyes (P=0.001 for both).
Figure 4 Correlation of glycosylated hemoglobin (HbA1c) and ganglion cell complex (GCC) parameters in both groups: (a) in group 1 (G1), and (b) in group 2 (G2).

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  Discussion Top


Most of the published work on the topic of retina in diabetes has investigated the effect of vascular changes on visual function, neglecting the effect of neuroretinal degenerative changes. However, currently, there are strong arguments that retinopathy should not be viewed as a vascular pathology in isolation but as a neurovascular pathology [6].

This study has been done to investigate the correlation of RNFL and GCC thickness with HbA1c in diabetic patients. The aim was to tackle the possibility of occurrence of these neuroretinal changes as an early introduction, which may even predate the microvascular changes, to more serious diabetic ocular complications.

According to this research methodology, the results have been categorized into four parts depending on the degree of RNFL and GCC thickness affection and correlation and FLV and GLV of GCC layer in relation to HbA1c level.

In the first part, we found that at HbA1c more than 9%, the thickness of RFNL and GCC experienced a significant thinning, which is a novel finding.

Moreover, in the second part, there was a statistically significantly lower thickness of average and temporal quadrants in the right eyes, and the inferior quadrant in both eyes in group 1 compared with group 2. In addition, there was a negative significant correlation between HbA1c and average, superior, inferior, and nasal RNFL quadrants in group 1.

These results concur with the results of Gundogan et al. [12], which showed that the average RNFL, superior and inferior quadrant thickness, and the superior half of the peripapillary RNFL (pRNFL) thickness were significantly thinner in diabetic patients compared with controls (P<0.05). Furthermore, there was a significant negative correlation of the level of HbA1c with the average and superior quadrant thickness of the RNFL (P<0.05) [12]. In a previous study by Dhasmana et al. [9], RNFL thinning was observed in the superotemporal (P=0.001) and superonasal sectors (P=0.031) around the optic disc in patients with DR. Moreover, Fahmy et al. [13] detected a significant decrease in pRNFL thickness in the superior and inferior quadrants of the right eye (P=0.001 and 0.039, respectively) and in the superior quadrant of the left eye (P=0.002) with impairment of glycemic control. Using Pearson’s correlation test, there was a significant negative correlation of RNFL thickness with HbA1c in the superior quadrant in both eyes. They concluded that impairment of glycemic control affects the pRNFL thickness. This may become a useful method to monitor the early retinal changes in diabetic patients. They also demonstrated a significant thinning in the RNFL in patients with HbA1c less than 7% (controlled DM) which has been increased in patients with HbA1c more than or equal to 7% (uncontrolled DM) [13].

Contrary to this, Nor-Sharina et al. [14], who used scanning laser polarimetry, found that the level of HbA1c had no significant relation with the reduction of RNFL thickness neither in their study nor in the other studies with which they compared their results with, such as the studies by Chihara et al. [15] and Peng et al. [16]. In the study by Borooah et al. [17], which was done on 30 patients with type II DM without DR, 30 patients with mild DR, and 30 healthy controls, the average RNFL thickness was 86.18±8.44 and 91.79±4.77 µm in diabetic patients and controls, respectively (P=0.002). The correlation of average RNFL thickness and GCC thickness was not statistically significant with the duration of diabetes and HbA1c value. They concluded that the neuroretinal changes occur before vascular changes of DR [17].

Regarding part three of this study results about GCC thickness affection by HbA1c, two statistically significant results were presented. First, group 1 showed a statistically significantly lower average and inferior quadrant thickness of GCC in the right eyes (median=88.35 and 87.62, respectively) than in group 2 (median=96.43 and 194.41, respectively). Moreover, a significant negative correlation between HbA1c and average, superior, and inferior GCC in both eyes was obtained among group 1. The study by Borooah et al. [17] showed also that the average GCC thickness was 80.15±5.78 µm in the non-DR group and 79.75±5.70 µm in the mild DR group (P=0.788). There was a statistically significant reduction in the mean GCC thickness in type II diabetes with non-DR or mild DR compared with the control group [17].

According to the study by Mahmoud et al. [18], there was a significant reduction in the superior and inferior GCC thickness in the diabetic group compared with the normal participants. The odds ratio in Alabdulwahhab [19] study for HbA1c was 1.995. Patients who have high HbA1c levels have 1.995 times more chances to develop DR than the control group (with confidence limits 1.690–2.353). Therefore, HbA1c variable plays a significant role in predicting the development of DR (P<0.001) [19]. In the study by Demir et al. [20], HbA1c level was significantly higher in patients with DR compared with controls. The GCC was thinner in patients with DM compared with controls, but the difference was not statistically significant [20].

Finally, in the last part related to FLV and GLV, two results were presented. First, the FLV in left eyes was statistically significantly higher in group 1 than in group 2. In addition, GLV was statistically significantly higher in group 1 in both eyes. Second, there was a significant positive correlation between HbA1c and FLV in both eyes in group 1. In contrast, HbA1c was found to be negatively correlated with FLV and GLV in both eyes in group 2. The study by Refai and Hassan [21] which augmented this point of view showed that the FLV% values in particular were abnormal in ∼70% of eyes with diabetes in comparison with normative data. This study also recommended considering FLV% as a reliable parameter for monitoring of severe progression of DME before permanent GCC damage starts to occur [21]. FLV% was found to be significantly higher in diabetic eyes by 22.2% more than in the normal eyes (P=0.024). No statistically significant difference was found for the diabetic and control groups regarding GLV% (P=0.160). Moreover, FLV% was found to be negatively correlated with HbA1c level (P=0.013) [8].

The main limitation of this study was the small sample size because we had chosen a highly selective group of patients who fulfilled our inclusion criteria. So, there is a further need for more studies on larger groups of diabetic eyes. This is suggested to be done for additional investigation of the RNFL and GCC thickness maps and its relation to HbA1c level and to assess the histopathology and pathophysiology of neurological loss patterns of these layers for more consolidation of our findings of RNFL and GCC thicknesses affection by HbA1c more than 9%.


  Conclusion and recommendations Top


The structure of the neuronal retinal layers (RNFL and GCC) was affected early by diabetes, which even preceded the retinal vascular changes and visual affection in occurrence in most of the studied patients. There was a statistically significant correlation of the thinning of most of RNFL and GCC quadrants with uncontrolled glucose with HbA1c more than 9%.

It is recommended to use the pRNFL and GCC thickness as early warning markers of retinopathy development by doing routine optic disc OCT with the routinely requested macular OCT in the diabetic ocular checkup and in monitoring of the newly diagnosed cases of DM. It should also not be neglected during the follow-up of diabetic patients on antihyperglycemic treatment with highly suspected DR or vasculopathy. Moreover, in uncontrolled diabetes with HbA1c more than 9%, we find it urgent for diabetic patient’s ophthalmologist and internist to continuously coordinate and share data for appropriate intervention and management.

Acknowledgements

The authors thank the chair Department of Ophthalmology, Beni-Suef University, and other faculty members for their assistance in carrying out this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Magliano DJ, Zimmet P, Shaw JE. Classification of diabetes mellitus and other categories of glucose intolerance. In: DeFronzo RA, editor. International textbook of diabetes mellitus. 4th ed. New Jersey, USA: Wiley-Blackwell 2015. 3–16  Back to cited text no. 1
    
2.
Sherwani SI, Khan HA, Ekhzaimy A, Masood A, Sakharkar MK. Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights 2016; 11:95–104.  Back to cited text no. 2
    
3.
Sahoo PK, Fiaz S. Conceptual analysis of diabetic retinopathy in Ayurveda. J Ayurveda Integr Med 2017; 8:122–131.  Back to cited text no. 3
    
4.
Kern TS, Barber AJ. Retinal ganglion cells in diabetes. J Physiol 2008; 586:4401–4408.  Back to cited text no. 4
    
5.
Duh EJ, Sun JK, Stitt AW. Diabetic retinopathy: current understanding, mechanisms, and treatment strategies. JCI Insight 2017; 2:e93751.  Back to cited text no. 5
    
6.
El-Hifnawy MA, Sabry KM, Gomaa AR, Hassan TA. Effect of diabetic retinopathy on retinal nerve fiber layer thickness. Delta J Ophthalmol 2016; 17:162–166.  Back to cited text no. 6
  [Full text]  
7.
Takis A, Alonistiotis D, Ioannou N, Kontou E, Mitsopoulou M, Papaconstantinou D. Follow-up of the retinal nerve fiber layer thickness of diabetic patients type 2, as a predisposing factor for glaucoma compared to normal subjects. Clin Ophthalmol 2017; 11:1135–1141.  Back to cited text no. 7
    
8.
Hegazy AI, Zedan RH, Macky TA, Esmat SM. Retinal ganglion cell complex changes using spectral domain optical coherence tomography in diabetic patients without retinopathy. Int J Ophthalmol 2017; 10:427–433.  Back to cited text no. 8
    
9.
Dhasmana R, Sah S, Gupta N. Study of retinal nerve fibre layer thickness in patients with diabetes mellitus using fourier domain optical coherence tomography. J Clin Diagn Res 2016; 10: NC05–NC09.  Back to cited text no. 9
    
10.
Weykamp C. HbA1c: a review of analytical and clinical aspects. Ann Lab Med 2013; 33:393–400.  Back to cited text no. 10
    
11.
American Diabetes Association. 6. Glycemic targets: standards of medical care in diabetes-2018. Diabetes Care 2018; 41:S55–S64.  Back to cited text no. 11
    
12.
Gundogan FC, Akay F, Uzun S, Yolcu U, Cagiltay E, Toyran S. Early neurodegeneration of the inner retinal layers in type 1 diabetes mellitus. Ophthalmologica 2016; 235:125–132.  Back to cited text no. 12
    
13.
Fahmy RM, Bhat RS, Al-Mutairi M, Aljaser FS, El-Ansary A. Correlation between glycemic control and peripapillary retinal nerve fiber layer thickness in Saudi type II diabetics. Clin Ophthalmol 2018; 12:419–425.  Back to cited text no. 13
    
14.
Nor-Sharina Y, Zunaina E, Shatriah I, Win-Mar K, Azriani A. Correlation of retinal nerve fibre layer thickness with HbA1c and oxidised LDL in non-proliferative diabetic retinopathy. J Diabetes Metab 2013; 4:1–6.  Back to cited text no. 14
    
15.
Chihara E, Matsuoka T, Ogura Y, Matsumura M. Retinal nerve fiber layer defect as an early manifestation of diabetic retinopathy. Ophthalmology 1993; 100:1147–1151.  Back to cited text no. 15
    
16.
Peng PH, Lin HS, Lin S. Nerve fibre layer thinning in patients with preclinical retinopathy. Can J Ophthalmol 2009; 44:417–422.  Back to cited text no. 16
    
17.
Borooah M, Nane YJ, Ekka J. Evaluation of thickness of retinal nerve fiber layer and ganglion cell layer with inner plexiform layer in patients without diabetic retinopathy and mild diabetic retinopathy in type 2 diabetes mellitus patients using spectral-domain optical coherence tomography. Int J Res Med Sci 2018; 6:2434–2439.  Back to cited text no. 17
    
18.
Mahmoud DA, Abdulwahab AM, Ali DA. Correlation of peripapillary retinal nerve fiber layer thickness and ganglion cell complex thickness with the severity of diabetic retinopathy. Delta J Ophthalmol 2018; 19:117–121.  Back to cited text no. 18
  [Full text]  
19.
Alabdulwahhab KM. Relationship between diabetic retinopathy and HbA1c in type 2 diabetics, Kingdom of Saudi Arabia. J Med Dent Sci 2019; 7:1–4.  Back to cited text no. 19
    
20.
Demir M, Oba E, Sensoz H, Ozdal E. Retinal nerve fiber layer and ganglion cell complex thickness in patients with type 2 diabetes mellitus. Indian J Ophthalmol 2014; 62:719–720.  Back to cited text no. 20
[PUBMED]  [Full text]  
21.
Refai T, Hassan AA. Gang lion cell complex changes with long-standing diabetic macular oedema among Egyptian diabetic patients: an optical coherence tomography study. J Egypt Ophthalmol Soc 2018; 111:25–32.  Back to cited text no. 21
    


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