Clinical Study Changes in Frequency-Doubling Perimetry .Changes in Frequency-Doubling Perimetry in

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  • Hindawi Publishing CorporationBioMed Research InternationalVolume 2013, Article ID 341269, 7 pages

    Clinical StudyChanges in Frequency-Doubling Perimetry in Patients withType I Diabetes prior to Retinopathy

    Isabel Pinilla,1 Antonio Ferreras,2 Miriam Idoipe,2 Ana I. Sanchez-Cano,3

    Diana Perez-Garcia,1 Laura X. Herrera,1 Maria J. Pinilla,4 and Emilio Abecia2

    1 Department of Ophthalmology, Hospital Clinico Universitario Lozano Blesa, Aragon Health Sciences Institute,50009 Zaragoza, Spain

    2Miguel Servet University Hospital, Aragon Health Sciences Institute, 50009 Zaragoza, Spain3 Department of Applied Physics, Zaragoza University, 50009 Zaragoza, Spain4Department of Cardiology, Hospital Clinico Universitario Lozano Blesa, Aragon Health Sciences Institute, 50009 Zaragoza, Spain

    Correspondence should be addressed to Antonio Ferreras;

    Received 21 July 2013; Revised 23 September 2013; Accepted 25 September 2013

    Academic Editor: Atsushi Mizota

    Copyright 2013 Isabel Pinilla et al. This is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Purpose. To evaluate the ability of frequency-doubling technology (FDT) perimetry in detecting visual field defects in youngadults with type I diabetes prior to retinopathy or with minor retinovascular changes. Methods. This comparative cross-sectionalstudy included 30 healthy subjects and 73 age-matched patients with type I diabetes mellitus. All subjects underwent a full ocularexamination including an FDTwith the threshold C-20-5 strategy. Only one eye per subject was randomly included in the statisticalanalysis. FDT results and time to perform the test were compared between the groups. Results. The mean age was 27.1 years inthe control group and 26.6 years in the diabetic group ( = 0.875). The mean period from the onset of diabetes was 12.6 6.7years, while minimal retinovascular changes were observed in 18 eyes. Mean deviation of FDT did not differ between the groups.Although global indices of FDT were within normal limits, pattern standard deviation of FDT was higher in the diabetic group( = 0.035). The area under the receiver operating characteristic curve was 0.647 for pattern standard deviation of FDT (standarderror = 0.052; = 0.017). Conclusion. FDT can detect retinal dysfunctions in diabetic patients prior to the onset of significantvascular complications.

    1. Introduction

    Diabetic retinopathy is the major cause of visual loss in thediabetic population, although it is not the only aspect ofvisual dysfunction in these patients. There is accumulatingevidence indicating that the impairment of retinal functionprecedes the earliest signs of vascular complications. Also,functional defects have been reported in animal models ofdiabetic retinopathy prior to the occurrence of any clinicallyvisible changes [1, 2]. Such defects are attributed to a decreasein nerve function and consist of alterations in oscillatorypotentials, pattern electroretinogram (ERG),multifocal ERG,S-cone ERG, and paired-flash ERG [310]. Other changesinclude reductions in dark adaptation, visually evokedresponses, contrast sensitivity, and optic nerve conductionvelocity [1113]. Additionally, abnormal colour sensation [14],

    prolongations in visually evoked response latencies [1522],and defects in the retinal nerve fiber layer [23] have beendetected at stages preceding detectable retinopathy.

    Some years ago, frequency-doubling technology (FDT)perimetry was introduced, a method for assessing contrastthreshold based on the spatial frequency-doubling illusionthat occurs when a low spatial frequency sine wave gratingis counterphased at a high temporal rate, resulting in thegratings appearing to have twice its original spatial frequency[2428]. Frequency-doubling illusion does not depend oncontrast reversal and any rapid temporal variation will doeither translation or pattern onset.Thus, localized visual fielddefects are tested as malfunctions of the temporal contrastbehaviour andmay contribute to the results obtainedwith theFDT perimeter.

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    White et al. [29] suggested that a cortical loss of temporalphase discrimination is the principal cause of the illusionand proposed that the mechanisms underlying the illusionresemble those underlying the detection of full-field flicker,which appears to be accomplished through themagnocellularpathway.Therefore, FDT can be abnormal not only in patientswith visual field defects, such as those found in glaucoma,but also in patients with impaired contrast sensitivity. Thethreshold contrast, at which a pattern of stripes is just visible,is a measure of a different visual function that can pick updeficits in diverse pathologies including retinal diseases [11,3032].The reduction in contrast sensitivity found in diabeticpatients can be a source of abnormal FDT [33].

    To our knowledge this is the first study aimed to evaluatethe efficacy of FDT in detecting functional impairment ofvision in patients with type I diabetes without retinopathy orwith minor retinovascular changes.

    2. Materials and Methods

    Thecomparative cross-sectional study protocol was approvedby the ethics committee of theMiguel Servet University Hos-pital and written consent was obtained from all participants.

    Thirty consecutive eyes of 30 healthy young adults and 73consecutive eyes of 73 patients with type I diabetes mellitusthat met the inclusion criteria were prospectively enrolled inthe study. Control eyes were selected from patients referredfor refraction and routine exploration without abnormalocular findings, hospital staff, and relatives of patients of ourhospital. Diabetic patients were recruited from those referredfor annual diabetic retinopathy screening.

    The following criteria were met in both groups: agebetween 15 and 45 years, no cardiac diseases or uncontrolledarterial hypertension (over 130/80mmHg), best-correctedvisual acuity of 20/30 or better (Snellen), Goldmann appla-nation tonometry lower than 20mmHg, refractive errorsless than 5 spherical diopters and 2 cylinder diopters, andtransparent ocularmedia (nuclear color/opalescence, corticalor posterior subcapsular lens opacity

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    Right eye

    Test duration: 4:16

    Left eye

    Test duration: 4:15

    32 32 32





    34 3432



    31 32 28





    32 2833







    Threshold (dB)

    Total deviation

    Pattern deviation

    Fixation errors: 0/6False positive errors: 0/6

    MD: +2.18 dBPSD: +3.01dB

    Fixation errors: 0/6False positive errors: 0/6

    MD: +1.95 dBPSD: +3.31dB

    False negative errors: 0/3False negative errors: 0/3

    P 5%5%P 3.99).

    3.1.3. Test Time. There were no differences in the test timesbetween both groups.The control group needed a mean timeof 4.33 0.3 minutes to perform the perimetry and the dia-betic group required 4.370.4minutes ( = 0.69). Neverthe-less, the time to perform the FDT tests depended on the yearswhich passed since the diagnosis of the disease. Patients withless than 10 years following diagnosis of diabetes requireda time of 4.21 0.4 minutes, while those with more than10 years required a time of 4.42 0.5minutes ( = 0.045).

    4. Discussion

    Visual dysfunctions occur in diabetic patients before obviousvasculopathy. Consequently, the vascular aberrations per seare not necessarily the cause of the visual losses. Since retinalneurons transduce visual signals, it follows that the loss ofneuronal function within the retina circuitry is likely to leadto visual impairment.Diabetes is known to have a direct effecton retinal neurons and, as a result, alterations in neuronalfunction could occur soon after the beginning of the diabetes[1, 2]. These neuropathological changes themselves may con-tribute to the development of the diabetic retinopathy.Abnor-malities in a wide range of electrophysiological tests havebeen found before vascular anomalies were detected. Thepresent study explored whether the FDT would be useful for

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    the individual patient in detecting such changes in neuronalfunction.

    FDT is a quick and efficient way of screening visualfield with a very good sensitivity and specificity [28]. Thisperimetry is most likely a probe of contrast sensitivity of themagnocellular pathway [29]. Contrast sensitivity is known tobe affected in diabetic patients and, therefore, FDT can be apromising psychophysical test candidate for the detection ofnot only glaucoma [37] but also other diseases such as dia-betic retinopathy.

    TheC-20-5 strategy tests the central 20 (1010 targets),4 per quadrantwithin the central 20, with one smaller centraltarget (5 diameter circle) projected on themacular region. Inour study, we used 45 fundus photographs centered on thefovea and the optic disc. Consequently, they should cover thearea of the retina assessed by FDT. We did not find changesin the number of altered FDT tests. This suggests that thediabetic patient might not already have detectable visual fielddefects.Thus, it is important to consider that the abnormalitycriterion for FDT was based on glaucoma patients [36].Hence, there will be a need for a new definition for patientswith diabetes, who are likely to have different visual fielddefects than patients with glaucoma.

    Although MD was similar between diabetic and normalgroups, there was a statistically significant difference in PSDvalues. This suggests that localized diminutions of retinalsensitivity occu