Skip to content

Advertisement

  • Research Article
  • Open Access
  • Open Peer Review

RETRACTED ARTICLE: Cental macular thickness in patients with type 2 diabetes mellitus without clinical retinopathy

BMC Ophthalmology201313:11

https://doi.org/10.1186/1471-2415-13-11

©  Demir et al.; licensee BioMed Central Ltd. 2013

  • Received: 2 October 2012
  • Accepted: 15 March 2013
  • Published:

The Retraction Note to this article has been published in BMC Ophthalmology 2015 15:167

Open Peer Review reports

Abstract

Background

An increase in macular thickness due to fluid accumulation in the macula in patients with diabetes mellitus. Optical coherence tomography (OCT) has been shown to be highly reproducible in measuring macular thickness in normal individuals and diabetic patients. OCT can detect subtle changes of macular thickness. The aim of this study is to compare central macular thickness (CMT) of diabetic patients with type 2 diabetes without clinical retinopathy and normal controls, in order to assess possible increased macular thickness associated with diabetes mellitus.

Methods

Optical coherence tomography (OCT) measurements were performed in 124 eyes of 62 subjects with diabetes mellitus without clinically retinopathy (study group: 39 female, 23 male, mean age: 55.06 ± 9.77 years) and in 120 eyes of 60 healthy subjects (control group: 35 female, 25 male, mean age: 55.78 ± 10.34 years). Blood biochemistry parameters were analyzed in all cases. The data for central macular thickness (at 1 mm) and the levels of the fasting plasma glucose and glycosylated hemoglobin (HbA1c) were compared in both groups.

Results

The mean central macular thickness was 232.12 ±24.41 μm in the study group and 227.19 ± 29.94 μm in the control group.

The mean HbA1c level was 8.92 ± 2.58% in the study group and 5.07 ± 0.70% in the control group (p=0.001). No statistically significant relationship was found between CMT, HbA1c, and fasting plasma glucose level in either group (p=0.05).

Conclusions

Central macular thickness was not significantly thicker in patients with type 2 diabetes without clinical retinopathy than in healthy subjects.

Keywords

  • Diabetes mellitus
  • Central macular thickness
  • Glycosylated hemoglobin
  • Fasting plasma glucose level

Background

Diabetic retinopathy is the leading cause of blindness in working aged adults in westernized countries. Diabetic macular edema (DME) has been reported at rates of 10% and occurs more frequently in type 2 diabetes mellitus than in type 1. Diabetic patients also have multiple risk factors for retinopathy, such as hyperglycemia and hypertension [1]. Their visual acuity is often dependent the central foveal involvement, perifoveal capillary blood flow velocity, severity of perifoveal capillary occlusion, and retinal thickness at the central fovea [2, 3]. The clinical findings of diabetic retinopathy are microaneurysms, soft exudates, accumulation of hard exudates, and neovascularisation.

Macular edema can develop at any stage of diabetic retinopathy. In the past, macular edema was diagnosed with slit-lamp view. Fundus fluorescein angiography provides guidance for treatment of macular edema. Optical coherence tomography (OCT) has been used for detection of macular edema secondary to different pathologies, such as diabetes mellitus, central or branched retinal vein occlusion, uveitis, and age related macular degeneration [4]–[11].

Methods

The central macular thickness (CMT) was measured in both groups by OCT (Optovue Inc. Co., RTVue 100 model, Fremont, CA). The CMT was measured after providing pupil dilation with tropicamide drops 2 times, 10 minutes before measurement (Tropicamide 1%, Alcon Lab. Inc, USA). Three measurements were taken from each patient after pupillary dilatation. Blood biochemical tests for glycosylated hemoglobin (HbA1c) and fasting plasma glucose levels were run on all patients. All cases underwent ophthalmological examinations including best corrected visual acuity (BCVA), anterior and posterior segment examinations under slit-lamp, intraocular pressure (IOP) (applanation tonometer model AT 900; Haag-Streit, Switzerland), and central macular thickness measured by OCT Visual acuity was measured with an Early Treatment Diabetic Retinopathy Study chart at 4 meters. Each subject gave written informed consent to participate in the study. Ethic Committee approval was obtained from local committee.

Participiants

The study group included 62 patients (124 eyes; 39 female, 23 male, mean age: 55.06 ± 9.77 years) who had type 2 diabetes mellitus without clinical retinopathy and a control group of 60 patients (120 eyes; 35 female, 25 male, mean age: 55.78 ± 10.34 years) (Table 1). Inclusion criteria for the study group included: no visible findings of diabetic retinopathy (hard-soft exudates, microaneurysms) on retina at slit-lamp fundus examination with a +78 D lens, type 2 diabetes mellitus, no other problems (such as hypertension, uveitis), and no history of ophthalmologic trauma, intravitreal injection, high refractive errors (spherical equivalent; between: +1.00 D to −1.00 D) or use of drugs(s) for retinal problems. Inclusion criteria for the control group patients included: no ophthalmologic or systemic problems, no history of intraocular surgery or treatment of the retina, and no high refractive errors (spherical equivalent: between −1.0 D to +1.0 D). Exclusion criteria for both groups were visible retinopathy or uveitis, hypertension, or previous ophthalmologic surgery. In the study group, the duration of diabetes mellitus ranged from 0 – 20 years and the average was 7.19 ± 4.87 years. Five patients were newly diagnosed, 19 patients had been diagnosed for 1–5 years, 23 patients had been diagnosed for 6–10 years, 9 patients had been diagnosed for 11–15 years, and 6 patients had been diagnosed for more than 15 years. In the study group; five patients were newly diagnosed, 49 patients were undergoing insulin treatment, and 8 patients were taking oral antidiabetic drugs (Table 2). Both groups were compared based on mean age, central macular thickness, fasting plasma glucose, and HbA1c levels.
Table 1

Demographic characteristics, values for central macular thickness (CMT), and biochemical analysis in patients with type 2 diabetes without clinical retinopathy

Parameters

Study group (n=62)

Control group (n=60)

p

BCVA

0.00 (log MAR)

0.00 (logMAR)

NS

IOP mmHg

17,8 ±2.3 mmHg

18.1 ±2.1 mmHg

NS

Age(year)

55.06±9.77

55.78±10.34

NS

Male/Female Gender

23/39

25/35

NS

CMTμm(±SD)

232.12±24.41

227.19±29.94

NS

HbA1c ( mean±SD)

8.92±2.58

5.07±0.70

0.001

Fasting blood glucose Average ±SD

202.14±104.78 (median:178 )

92.17±7.75 (median:92)

0.001

BCVA: Best corrected visual acuity, IOP: Intraocular pressure, CMT: Central macular thickness, μm:micrometer, SD: standard deviation, logMAR: logarithm of the minimum angle of resolution, HbA1c: glycosylated hemoglobin, n: number of patients, logMAR: logarithm of the minimum angle of resolution, NS: Non significant; Study group: Patients with type 2 diabetes without clinical retinopathy; Control group: healthy controls.

Table 2

Duration and treatment of diabetes mellitus in patients with type 2 diabetes without clinical retinopathy

Duration of DM

n (=62)

%

New diagnosis

5

8.1

1-5 years

19

30.6

6-10 years

23

37.1

11-15 years

9

14.5

>15 years

6

9.7

Insulin treatment

49

79

OAD (oral anti-diabetic drug)

8

12.9

DM: Diabetes mellitus, n: number of patients.

Statistical analysis

The NCSS (Number Cruncher Statistical System) 2007 and the PASS 2008 Statistical Software (Utah, USA) programs were used to evaluate the results of the study.

Descriptive statistical methods (mean, standard deviation) and Student’s t- test were used together to compare the data from the two groups and the parameters that showed normal distribution. The Mann Whitney U test was used to compare parameters of the two groups that did not show normal distribution. A Chi-square test was used to compare the quality of the data. Pearson correlation analyses were conducted to evaluate the relationship between the parameters showing normal distribution and Spearman’s rho correlation analyses have been used to evaluate correlation between the parameters not showing normal distribution. A value of p<0.05 was considered significant.

Results

Best corrected vision (BCVA) was 0.00 (log MAR) in both groups. No significant differences were found for the mean age, IOP, or gender distribution (Table 1).

The mean HbA1c level was 8.92 ± 2.58% in the study group, and 5.07 ± 0.70% in the control group. The mean level of HbA1c was statistically higher in the study group than in the control group (Table 1, p=0.001). Fasting plasma glucose level was statistically higher in the study group than in the control group (Table 1, p=0.01). The duration of diabetes mellitus was 7.19 ± 4.8 (range: 0–20) years. The mean of CMT was 232.12 ± 24.41 μm in the study group and 227.19 ± 29.94 μm in the control group (Table 1). The CMT was thicker in the study group than in the control group but this difference was not statistically significant.

No relationship was found between CMT and fasting plasma glucose level in the study (p=0.483) and control (p=0.399) groups. No relationship was found between CMT and HbA1c level in the study (p=0.550), and control (p=0.997; Table 3).
Table 3

Relationship between central macular thickness (CMT), glycosylated hemoglobin (HbA1c), and fasting blood glucose levels in patients with type 2 diabetes without clinical retinopathy

Parameters

Study group

Study group

Control group

Control group

 

r

p

r

p

CMT-HbA1c

−0.077

NS

0.001

NS

CMT-Fasting glucose level

−0.091

NS

0.011

NS

CMT: Central macular thickness, HbA1c: glycosylated hemoglobin, p; statistic value, r: relation between two variables.

NS: Non significant; Study group: Patients with type 2 diabetes without clinical retinopathy; Control group: healthy controls.

Discussion

We found no studies in the literature which reviewed CMT, fasting plasma glucose level, and level of HbA1c less than HbA1c 8%.

Several previous studies [12]–[17] determined that optical coherence tomography can help in the evaluation of macular edema in diabetic or non-diabetic patients, and also help in the follow-up of the patients during treatment to establish quantitative or qualitative responses to therapy.

We reviewed the relationship between central macular thickness, HbA1c, and fasting plasma glucose levels in patients with type 2 diabetes without clinical diabetic retinopathy. Optical Coherence Tomography (OCT) was used for objective measurement and monitoring of central macular thickness. Browning and Hee, et al. [18, 19] described that a change in the OCT measurements greater than 10% of the baseline thickness is likely to represent a true change in macular thickness. Glycosylated hemoglobin is a parameter that can be used to follow up hyperglycemia over the long term. Moon, at al [20] suggested that a high baseline HbA1c and a large reduction in HbA1c were risk factors for increase in macular thickness. Yeung, et al [21], showed that HbA1c level positively correlated with macular thickness in patients with type1 and 2 diabetes of10 or more years’ duration without diabetic macular edema. Chou, Moreira at al [22]. showed that a HbA1c level of 8% or above was associated with an increase in macular thickness in diabetic patients with diabetic retinopathy. Yeung, at al. [21]–[23] concluded that meticulous diabetes control may slow the progression of early diabetic retinopathy and may play an important role in preventing macular dysfunction. In type 1 and 2 diabetes patients, strict follow-up of plasma glucose level could reduce the progression and development of diabetic retinopathy.

The purpose of this study was to examine central macular thickness in patients with type 2 diabetes mellitus without retinopathy. This study showed the following four results: 1) The mean central macular thickness is thicker in diabetic patients without diabetic retinopathy than in healthy subjects, but this difference was not statistically significant; 2) No positive relationship was found between fasting plasma glucose level and the central macular thickness in patients with diabetes mellitus without retinopathy; 3) Central macular thickness was not increased by mild or high levels of HbA1c (8.92 ± 2.59%); and 4) Central macular thickness was not affected by the duration of diabetes mellitus in patients with diabetes type 2 without retinopathy. There are limitations to our study. One of these is the small sample size in both groups and another is that no patients had diabetes mellitus for longer than 20 years.

Conclusion

Our opinion is that the truly effective parameter on macular thickness is vascular permeability in patients with diabetes mellitus.

In this study, glycosylated HbA1c and fasting plasma glucose levels were significantly higher in diabetic patients without retinopathy than in the control group, although there was no difference in central macular thickness between the two groups.

Notes

Declarations

Acknowledgements

Thanks to Celeste Krauss (and her team) who provided writing in good medical English CEO of http://www.Mededit.net

Thanks to Bendisah Karaer for helping to transfer of participiants to room of Optic Coherence Tomography.

Authors’ Affiliations

(1)
Sisli Etfal Training and Research Hospital, Eye Clinic, Karayolları Mah. Abdi ipekci bulvarı. N0:32 Avrupa tem konutları 28. Blok. Daire:14. 34250 GOP, Sisli, Istanbul, 34400, Turkey

References

  1. Girach A, Lund-Andersen H: Diabetic macular oedema: a clinical overview. Int J Clin Pract. 2007, 61: 88-97. 10.1111/j.1742-1241.2006.01211.x.View ArticlePubMedGoogle Scholar
  2. Gardner TW, Larsen M, Girach A, Zhi X: Protein Kinase C Diabetic Retinopathy Study (PKC-DRS2) Study Group. Diabetic macular oedema and visual loss: relationship to location, severity and duration. Acta Ophthalmol. 2009, 87: 709-713. 10.1111/j.1755-3768.2009.01545.x.View ArticlePubMedGoogle Scholar
  3. Sakata K, Funatsu H, Harino S, Noma H, Hori S: Relationship of macular microcirculation and retinal thickness with visual acuity in diabetic macular edema. Ophthalmology. 2007, 114: 2061-2069. 10.1016/j.ophtha.2007.01.003.View ArticlePubMedGoogle Scholar
  4. Yahia SB, Kahloun R, Jelliti B, Khairallah M: Branch retinal artery occlusion associated with Behçet disease. Ocul Immunol Inflamm. 2011, 19: 293-295. 10.3109/09273948.2011.582219.View ArticlePubMedGoogle Scholar
  5. Ogino K, Tsujikawa A, Nakamura H, Miyamoto K, Murakami T, Muraoka Y, Yoshimura N: Focal macular electroretinogram in macular edema secondary to central retinal vein occlusion. Invest Ophthalmol Vis Sci. 2011, 52: 3514-3520. 10.1167/iovs.10-7142.View ArticlePubMedGoogle Scholar
  6. Browning DJ, McOwen MD, Bowen RM, O'Marah TL: Comparison of the clinical diagnosis of diabetic macular edema with diagnosis by optical coherence tomography. Ophthalmology. 2004, 111: 712-715. 10.1016/j.ophtha.2003.06.028.View ArticlePubMedGoogle Scholar
  7. Virgili G, Menchini F, Murro V, Peluso E, Rosa F, Casazza G: Optical coherence tomography (OCT) for detection of macular oedema in patients with diabetic retinopathy. Cochrane Database Syst Rev. 2011, 7: CD008081-PubMedGoogle Scholar
  8. Ibrahim MA, Sepah YJ, Symons RC, Channa R, Hatef E, Khwaja A: Spectral- and time-domain optical coherence tomography measurements of macular thickness in normal eyes and in eyes with diabetic macular edema. Eye (Lond). 2012, 26: 454-462. 10.1038/eye.2011.293.View ArticleGoogle Scholar
  9. Medina FJ, Callén CI, Rebolleda G, Muñoz-Negrete FJ, Callén MJ, Valle FG: Use of Nonmydriatic Spectral-Domain Optical Coherence Tomography for Diagnosing Diabetic Macular Edema. Am J Ophthalmol. 2012, 153: 536-543. 10.1016/j.ajo.2011.08.008.View ArticlePubMedGoogle Scholar
  10. Suzuma K, Yamada Y, Liu M, Tsuiki E, Fujikawa A, Kitaoka T: Comparing central retinal thickness in diabetic macular edema measured by two different spectral-domain optical coherence tomography devices. Jpn J Ophthalmol. 2011, 55: 620-624. 10.1007/s10384-011-0085-4.View ArticlePubMedGoogle Scholar
  11. Kwon SI, Hwang DJ, Seo JY, Park IW: Evaluation of changes of macular thickness in diabetic retinopathy after cataract surgery. Korean J Ophthalmol. 2011, 25: 238-242. 10.3341/kjo.2011.25.4.238.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Udaondo P, Díaz-Llopis M, García-Delpech S, Salom D, Romero FJ: Intravitreal plasmin without vitrectomy for macular edema secondary to branch retinal vein occlusion. Arch Ophthalmol. 2011, 129: 283-287. 10.1001/archophthalmol.2011.8.View ArticlePubMedGoogle Scholar
  13. Moreira RO, Trujillo FR, Meirelles RM, Ellinger VC, Zagury L: Use of optical coherence tomography (OCT) and indirect ophthalmoscopy in the diagnosis of macular edema in diabetic patients. Int Ophthalmol. 2001, 24: 331-336.View ArticlePubMedGoogle Scholar
  14. Schneeberg AE, Göbel W: Diagnosis and follow-up of non-diabetic macular edema with optical coherence tomography (OCT). Ophthalmologe. 2003, 100: 960-966. 10.1007/s00347-003-0822-2.View ArticlePubMedGoogle Scholar
  15. Song JH, Lee JJ, Lee SJ: Comparison of the short-term effects of intravitreal triamcinolone acetonide and bevacizumab injection for diabetic macular edema. Korean J Ophthalmol. 2011, 25: 156-160. 10.3341/kjo.2011.25.3.156.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Takatsuna Y, Yamamoto S, Nakamura Y, Tatsumi T, Arai M, Mitamura Y: Long-term therapeutic efficacy of the subthreshold micropulse diode laser photocoagulation for diabetic macular edema. Jpn J Ophthalmol. 2011, 55: 365-369. 10.1007/s10384-011-0033-3.View ArticlePubMedGoogle Scholar
  17. Vemala R, Koshy S, Sivaprasad S: Qualitative and quantitative OCT response of diffuse diabetic macular oedema to macular laser photocoagulation. Eye (Lond). 2011, 25: 901-908. 10.1038/eye.2011.84.View ArticleGoogle Scholar
  18. Browning DJ, Fraser CM, Propst BW: The variation in optical coherence tomography-measured macular thickness in diabetic eyes without clinical macular edema. Am J Ophthalmol. 2008, 145: 889-893. 10.1016/j.ajo.2008.01.007.View ArticlePubMedGoogle Scholar
  19. Hee MR, Puliafito CA, Wong C, Duker JS, Reichel E, Rutledge B: Quantitative assessment of macular edema with optical coherence tomography. Arch Ophthalmol. 1995, 113: 1019-1029. 10.1001/archopht.1995.01100080071031.View ArticlePubMedGoogle Scholar
  20. Moon SW, Kim HY, Kim SW, Oh J, Huh K, Oh IK: The change of macular thickness measured by optical coherence tomography in relation to glycemic control in diabetic patients. Graefes Arch Clin Exp Ophthalmol. 2011, 249: 839-848. 10.1007/s00417-010-1562-z.View ArticlePubMedGoogle Scholar
  21. Yeung L, Sun CC, Ku WC, Chuang LH, Chen CH, Huang BY: Associations between chronic glycosylated haemoglobin (HbA1c) level and macular volume in diabetes patients without macular oedema. Acta Ophthalmol. 2010, 88: 753-758. 10.1111/j.1755-3768.2009.01711.x.View ArticlePubMedGoogle Scholar
  22. Chou TH, Wu PC, Kuo JZ, Lai CH, Kuo CN: Relationship of diabetic macular oedema with glycosylated haemoglobin. Eye (Lond). 2009, 23: 1360-1363. 10.1038/eye.2008.279.View ArticleGoogle Scholar
  23. Rosenstock J, Friberg T, Raskin P: Effect of glycemic control on microvascular complications in patients with type I diabetes mellitus. Am J Med. 1986, 81: 1012-1018. 10.1016/0002-9343(86)90398-0.View ArticlePubMedGoogle Scholar

    24. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2415/13/11/prepub

Copyright

© Demir et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement

BMC Ophthalmology

ISSN: 1471-2415

Contact us