A Girach

AE Schneeberg

Burcu Dirim

DJ Browning

Efe Can

Erhan Ozdal

Ersin Oba

FJ Medina

G Virgili

J Rosenstock

JH Song

K Ogino

K Sakata

K Suzuma

L Yeung

MA Ibrahim

Mehmet Demir

MR Hee

P Udaondo

R Vemala

RO Moreira

SB Yahia

SI Kwon

SW Moon

TH Chou

TW Gardner

Y Takatsuna

BMC Ophthalmology

Crossref

Demir et al. BMC Ophthalmology 2013, 13:11http://www.biomedcentral.com/1471-2415/13/11RESEARCH ARTICLE Open AccessCental macular thickness in patients with type 2diabetes mellitus without clinical retinopathyMehmet Demir*, Ersin Oba, Burcu Dirim, Erhan Ozdal and Efe Can EAbstractBackground: An increase in macular thickness due to fluid accumulation in the macula in patients with diabetesmellitus. Optical coherence tomography (OCT) has been shown to be highly reproducible in measuring macularthickness in normal individuals and diabetic patients. OCT can detect subtle changes of macular thickness. The aimof this study is to compare central macular thickness (CMT) of diabetic patients with type 2 diabetes without clinicalretinopathy and normal controls, in order to assess possible increased macular thickness associated with diabetesmellitus.Methods: Optical coherence tomography (OCT) measurements were performed in 124 eyes of 62 subjects withdiabetes mellitus without clinically retinopathy (study group: 39 female, 23 male, mean age: 55.06 ± 9.77 years) andin 120 eyes of 60 healthy subjects (control group: 35 female, 25 male, mean age: 55.78 ± 10.34 years). Bloodbiochemistry parameters were analyzed in all cases. The data for central macular thickness (at 1 mm) and the levelsof 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 inthe 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). Nostatistically significant relationship was found between CMT, HbA1c, and fasting plasma glucose level in eithergroup (p=0.05).Conclusions: Central macular thickness was not significantly thicker in patients with type 2 diabetes withoutclinical retinopathy than in healthy subjects.Keywords: Diabetes mellitus, Central macular thickness, Glycosylated hemoglobin, Fasting plasma glucose levelCTED ARTICLBackgroundDiabetic retinopathy is the leading cause of blindness inworking aged adults in westernized countries. Diabeticmacular edema (DME) has been reported at rates of 10%and occurs more frequently in type 2 diabetes mellitus thanin type 1. Diabetic patients also have multiple risk factorsfor retinopathy, such as hyperglycemia and hypertension[1]. Their visual acuity is often dependent the central fovealinvolvement, perifoveal capillary blood flow velocity, sever-ity of perifoveal capillary occlusion, and retinal thickness atthe central fovea [2,3]. The clinical findings of diabetic re-tinopathy are microaneurysms, soft exudates, accumulationof hard exudates, and neovascularisation.RETRA* Correspondence: ersinoba@yahoo.comSisli Etfal Training and Research Hospital, Eye Clinic, Karayolları Mah. Abdiipekci bulvarı. N0:32 Avrupa tem konutları 28. Blok. Daire:14. 34250 GOP, Sisli,Istanbul 34400, Turkey© 2013 Demir et al.; licensee BioMed Central LCommons Attribution License (http://creativecreproduction in any medium, provided the orMacular edema can develop at any stage of diabeticretinopathy. In the past, macular edema was diagnosedwith slit-lamp view. Fundus fluorescein angiography pro-vides guidance for treatment of macular edema. Opticalcoherence tomography (OCT) has been used for detectionof macular edema secondary to different pathologies, suchas diabetes mellitus, central or branched retinal vein occlu-sion, uveitis, and age related macular degeneration [4–11].MethodsThe central macular thickness (CMT) was measured inboth groups by OCT (Optovue Inc. Co., RTVue 100 model,Fremont, CA). The CMT was measured after providingpupil dilation with tropicamide drops 2 times, 10 minutesbefore measurement (Tropicamide 1%, Alcon Lab. Inc,USA). Three measurements were taken from each patienttd. This is an Open Access article distributed under the terms of the Creativeommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andiginal work is properly cited.Table 1 Demographic characteristics, values for central macular thickness (CMT), and biochemical analysis in patientswith type 2 diabetes without clinical retinopathyParameters Study group (n=62) Control group (n=60) pBCVA 0.00 (log MAR) 0.00 (logMAR) NSIOP mmHg 17,8 ±2.3 mmHg 18.1 ±2.1 mmHg NSAge(year) 55.06±9.77 55.78±10.34 NSMale/Female Gender 23/39 25/35 NSCMTμm(±SD) 232.12±24.41 227.19±29.94 NSHbA1c ( mean±SD) 8.92±2.58 5.07±0.70 0.001Fasting blood glucose Average ±SD 202.14±104.78 (median:178 ) 92.17±7.75 (median:92) 0.001BCVA: Best corrected visual acuity, IOP: Intraocular pressure, CMT: Central macular thickness, μm:micrometer, SD: standard deviation, logMAR: logarithm of theminimum 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.Demir et al. BMC Ophthalmology 2013, 13:11 Page 2 of 4http://www.biomedcentral.com/1471-2415/13/11LEafter pupillary dilatation. Blood biochemical tests forglycosylated hemoglobin (HbA1c) and fasting plasmaglucose levels were run on all patients. All cases under-went ophthalmological examinations including bestcorrected visual acuity (BCVA), anterior and posteriorsegment examinations under slit-lamp, intraocular pres-sure (IOP) (applanation tonometer model AT 900;Haag-Streit, Switzerland), and central macular thicknessmeasured by OCT Visual acuity was measured with anEarly Treatment Diabetic Retinopathy Study chart at 4meters. Each subject gave written informed consent toparticipate in the study. Ethic Committee approval wasobtained from local committee.ParticipiantsThe study group included 62 patients (124 eyes; 39female, 23 male, mean age: 55.06 ± 9.77 years) who hadtype 2 diabetes mellitus without clinical retinopathy anda control group of 60 patients (120 eyes; 35 female, 25male, mean age: 55.78 ± 10.34 years) (Table 1). Inclusioncriteria for the study group included: no visible findings ofdiabetic retinopathy (hard-soft exudates, microaneurysms)on retina at slit-lamp fundus examination with a +78 Dlens, type 2 diabetes mellitus, no other problems (such ashypertension, uveitis), and no history of ophthalmologictrauma, intravitreal injection, high refractive errors (sphe-rical equivalent; between: +1.00 D to −1.00 D) or use ofRACTETable 2 Duration and treatment of diabetes mellitus inpatients with type 2 diabetes without clinical retinopathyDuration of DM n (=62) %New diagnosis 5 8.11-5 years 19 30.66-10 years 23 37.111-15 years 9 14.5>15 years 6 9.7Insulin treatment 49 79OAD (oral anti-diabetic drug) 8 12.9DM: Diabetes mellitus, n: number of patients.RETdrugs(s) for retinal problems. Inclusion criteria for thecontrol group patients included: no ophthalmologic orsystemic problems, no history of intraocular surgery ortreatment of the retina, and no high refractive errors(spherical equivalent: between −1.0 D to +1.0 D). Exclu-sion criteria for both groups were visible retinopathy oruveitis, hypertension, or previous ophthalmologic surgery.In the study group, the duration of diabetes mellitusranged from 0 – 20 years and the average was 7.19 ± 4.87years. Five patients were newly diagnosed, 19 patients hadbeen diagnosed for 1–5 years, 23 patients had been diag-nosed for 6–10 years, 9 patients had been diagnosed for11–15 years, and 6 patients had been diagnosed for morethan 15 years. In the study group; five patients were newlydiagnosed, 49 patients were undergoing insulin treatment,and 8 patients were taking oral antidiabetic drugs (Table 2).Both groups were compared based on mean age, centralmacular thickness, fasting plasma glucose, and HbA1c levels.Statistical analysisThe NCSS (Number Cruncher Statistical System) 2007and the PASS 2008 Statistical Software (Utah, USA) pro-grams were used to evaluate the results of the study.Descriptive statistical methods (mean, standard de-viation) and Student’s t- test were used together to com-pare the data from the two groups and the parametersthat showed normal distribution. The Mann Whitney UD ARTICTable 3 Relationship between central macular thickness(CMT), glycosylated hemoglobin (HbA1c), and fastingblood glucose levels in patients with type 2 diabeteswithout clinical retinopathyParameters StudygroupStudygroupControlgroupControlgroupr p r pCMT-HbA1c −0.077 NS 0.001 NSCMT-Fasting glucose level −0.091 NS 0.011 NSCMT: Central macular thickness, HbA1c: glycosylated hemoglobin, p; statisticvalue, r: relation between two variables.NS: Non significant; Study group: Patients with type 2 diabetes without clinicalretinopathy; Control group: healthy controls.Demir et al. BMC Ophthalmology 2013, 13:11 Page 3 of 4http://www.biomedcentral.com/1471-2415/13/11test was used to compare parameters of the two groupsthat did not show normal distribution. A Chi-square testwas used to compare the quality of the data. Pearsoncorrelation analyses were conducted to evaluate the rela-tionship between the parameters showing normal distri-bution and Spearman’s rho correlation analyses havebeen used to evaluate correlation between the parame-ters not showing normal distribution. A value of p<0.05was considered significant.ResultsBest corrected vision (BCVA) was 0.00 (log MAR) inboth groups. No significant differences were found forthe mean age, IOP, or gender distribution (Table 1).The mean HbA1c level was 8.92 ± 2.58% in the studygroup, and 5.07 ± 0.70% in the control group. The meanlevel of HbA1c was statistically higher in the study groupthan in the control group (Table 1, p=0.001). Fastingplasma glucose level was statistically higher in the studygroup than in the control group (Table 1, p=0.01). Theduration of diabetes mellitus was 7.19 ± 4.8 (range: 0–20) years. The mean of CMT was 232.12 ± 24.41 μm inthe study group and 227.19 ± 29.94 μm in the controlgroup (Table 1). The CMT was thicker in the studygroup than in the control group but this difference wasnot statistically significant.No relationship was found between CMT and fastingplasma glucose level in the study (p=0.483) and control(p=0.399) groups. No relationship was found betweenCMT and HbA1c level in the study (p=0.550), and con-trol (p=0.997; Table 3).DiscussionWe found no studies in the literature which reviewedCMT, fasting plasma glucose level, and level of HbA1cless than HbA1c 8%.Several previous studies [12–17] determined that opticalcoherence tomography can help in the evaluation of macu-lar edema in diabetic or non-diabetic patients, and alsohelp in the follow-up of the patients during treatment toestablish quantitative or qualitative responses to therapy.We reviewed the relationship between central macularthickness, HbA1c, and fasting plasma glucose levels in pa-tients with type 2 diabetes without clinical diabetic retino-pathy. Optical Coherence Tomography (OCT) was usedfor objective measurement and monitoring of centralmacular thickness. Browning and Hee, et al. [18,19] de-scribed that a change in the OCT measurements greaterthan 10% of the baseline thickness is likely to represent atrue change in macular thickness. Glycosylated hemoglobinis a parameter that can be used to follow up hyperglycemiaover the long term. Moon, at al [20] suggested that a highbaseline HbA1c and a large reduction in HbA1c were riskfactors for increase in macular thickness. Yeung, et al [21],RETRACTEshowed that HbA1c level positively correlated with macu-lar thickness in patients with type1 and 2 diabetes of10 ormore 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 thick-ness in diabetic patients with diabetic retinopathy. Yeung,at al. [21–23] concluded that meticulous diabetes controlmay slow the progression of early diabetic retinopathy andmay play an important role in preventing macular dysfunc-tion. In type 1 and 2 diabetes patients, strict follow-up ofplasma glucose level could reduce the progression and de-velopment of diabetic retinopathy.The purpose of this study was to examine central macu-lar thickness in patients with type 2 diabetes mellitus with-out retinopathy. This study showed the following fourresults: 1) The mean central macular thickness is thickerin diabetic patients without diabetic retinopathy than inhealthy subjects, but this difference was not statisticallysignificant; 2) No positive relationship was found betweenfasting plasma glucose level and the central macular thick-ness in patients with diabetes mellitus without retino-pathy; 3) Central macular thickness was not increased bymild or high levels of HbA1c (8.92 ± 2.59%); and 4) Cen-tral macular thickness was not affected by the duration ofdiabetes mellitus in patients with diabetes type 2 withoutretinopathy. There are limitations to our study. One ofthese is the small sample size in both groups and ano-ther is that no patients had diabetes mellitus for longerthan 20 years.ConclusionOur opinion is that the truly effective parameter onmacular thickness is vascular permeability in patientswith diabetes mellitus.In this study, glycosylated HbA1c and fasting plasmaglucose levels were significantly higher in diabetic patientswithout retinopathy than in the control group, althoughthere was no difference in central macular thickness be-tween the two groups.Competing interestsThe authors have no finacial competing interests.Authors’ contributionsAll authors conceived of and designed the experimental protocol. MD andEO contributed to the study design and did critical revision of themanuscript for important intellectual content. MD, EO and BD participated inthe eye examinations. EO and EC collected the data. All authors read andapproved the final manuscript.AcknowledgementsThanks to Celeste Krauss (and her team) who provided writing in goodmedical English CEO of www.Mededit.netThanks to Bendisah Karaer for helping to transfer of participiants to room ofOptic Coherence Tomography.Received: 2 October 2012 Accepted: 15 March 2013Published: 9 April 2013D ARTICLEDemir et al. BMC Ophthalmology 2013, 13:11 Page 4 of 4http://www.biomedcentral.com/1471-2415/13/11D ARTICLEReferences1. Girach A, Lund-Andersen H: Diabetic macular oedema: a clinical overview.Int J Clin Pract 2007, 61:88–97.2. Gardner TW, Larsen M, Girach A, Zhi X: Protein Kinase C DiabeticRetinopathy Study (PKC-DRS2) Study Group. Diabetic macular oedemaand visual loss: relationship to location, severity and duration. ActaOphthalmol 2009, 87:709–713.3. Sakata K, Funatsu H, Harino S, Noma H, Hori S: Relationship of macularmicrocirculation and retinal thickness with visual acuity in diabeticmacular edema. Ophthalmology 2007, 114:2061–2069.4. Yahia SB, Kahloun R, Jelliti B, Khairallah M: Branch retinal artery occlusionassociated with Behçet disease. Ocul Immunol Inflamm 2011, 19:293–295.5. Ogino K, Tsujikawa A, Nakamura H, Miyamoto K, Murakami T, Muraoka Y,Yoshimura N, et al: Focal macular electroretinogram in macular edemasecondary to central retinal vein occlusion. Invest Ophthalmol Vis Sci 2011,52:3514–3520.6. Browning DJ, McOwen MD, Bowen RM Jr, O'Marah TL: Comparison of theclinical diagnosis of diabetic macular edema with diagnosis by opticalcoherence tomography. Ophthalmology 2004, 111:712–715.7. Virgili G, Menchini F, Murro V, Peluso E, Rosa F, Casazza G: Opticalcoherence tomography (OCT) for detection of macular oedema inpatients with diabetic retinopathy. Cochrane Database Syst Rev 2011,7:CD008081.8. Ibrahim MA, Sepah YJ, Symons RC, Channa R, Hatef E, Khwaja A, et al:Spectral- and time-domain optical coherence tomographymeasurements of macular thickness in normal eyes and in eyes withdiabetic macular edema. Eye (Lond) 2012, 26:454–462.9. Medina FJ, Callén CI, Rebolleda G, Muñoz-Negrete FJ, Callén MJ, Valle FG:Use of Nonmydriatic Spectral-Domain Optical Coherence Tomographyfor Diagnosing Diabetic Macular Edema. Am J Ophthalmol 2012,153:536–543.10. Suzuma K, Yamada Y, Liu M, Tsuiki E, Fujikawa A, Kitaoka T: Comparingcentral retinal thickness in diabetic macular edema measured by twodifferent spectral-domain optical coherence tomography devices.Jpn J Ophthalmol 2011, 55:620–624.11. Kwon SI, Hwang DJ, Seo JY, Park IW: Evaluation of changes of macularthickness in diabetic retinopathy after cataract surgery. Korean JOphthalmol 2011, 25:238–242.12. Udaondo P, Díaz-Llopis M, García-Delpech S, Salom D, Romero FJ:Intravitreal plasmin without vitrectomy for macular edema secondary tobranch retinal vein occlusion. Arch Ophthalmol 2011, 129:283–287.13. Moreira RO, Trujillo FR, Meirelles RM, Ellinger VC, Zagury L: Use of opticalcoherence tomography (OCT) and indirect ophthalmoscopy in thediagnosis of macular edema in diabetic patients. Int Ophthalmol 2001,24:331–336.14. Schneeberg AE, Göbel W: Diagnosis and follow-up of non-diabeticmacular edema with optical coherence tomography (OCT).Ophthalmologe 2003, 100:960–966.15. Song JH, Lee JJ, Lee SJ: Comparison of the short-term effects ofintravitreal triamcinolone acetonide and bevacizumab injection fordiabetic macular edema. Korean J Ophthalmol 2011, 25:156–160.16. Takatsuna Y, Yamamoto S, Nakamura Y, Tatsumi T, Arai M, Mitamura Y:Long-term therapeutic efficacy of the subthreshold micropulse diodelaser photocoagulation for diabetic macular edema. Jpn J Ophthalmol2011, 55:365–369.17. Vemala R, Koshy S, Sivaprasad S: Qualitative and quantitative OCTresponse of diffuse diabetic macular oedema to macular laserphotocoagulation. Eye (Lond) 2011, 25:901–908.18. Browning DJ, Fraser CM, Propst BW: The variation in optical coherencetomography-measured macular thickness in diabetic eyes withoutclinical macular edema. Am J Ophthalmol 2008, 145:889–893.19. Hee MR, Puliafito CA, Wong C, Duker JS, Reichel E, Rutledge B, et al:Quantitative assessment of macular edema with optical coherencetomography. Arch Ophthalmol 1995, 113:1019–1029.20. Moon SW, Kim HY, Kim SW, Oh J, Huh K, Oh IK: The change of macularthickness measured by optical coherence tomography in relation toglycemic control in diabetic patients. Graefes Arch Clin Exp Ophthalmol2011, 249:839–848.21. Yeung L, Sun CC, Ku WC, Chuang LH, Chen CH, Huang BY, et al:Associations between chronic glycosylated haemoglobin (HbA1c) levelRETRACTEand macular volume in diabetes patients without macular oedema.Acta Ophthalmol 2010, 88:753–758.22. Chou TH, Wu PC, Kuo JZ, Lai CH, Kuo CN: Relationship of diabetic macularoedema with glycosylated haemoglobin. Eye (Lond) 2009, 23:1360–1363.23. Rosenstock J, Friberg T, Raskin P: Effect of glycemic control onmicrovascular complications in patients with type I diabetes mellitus.Am J Med 1986, 81:1012–1018.doi:10.1186/1471-2415-13-11Cite this article as: Demir et al.: Cental macular thickness in patientswith type 2 diabetes mellitus without clinical retinopathy. BMCOphthalmology 2013 13:11.Submit your next manuscript to BioMed Centraland take full advantage of: • Convenient online submission• Thorough peer review• No space constraints or color ﬁgure charges• Immediate publication on acceptance• Inclusion in PubMed, CAS, Scopus and Google Scholar• Research which is freely available for redistributionSubmit your manuscript at www.biomedcentral.com/submit

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

https://bmcophthalmol.biomedcentral.com/track/pdf/10.1186/1471-2415-13-11?site=bmcophthalmol.biomedcentral.com

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

Abstract

Similar works

Full text

Available Versions

Crossref