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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 109  |  Issue : 1  |  Page : 26-31

Macular sensitivity in areas of capillary nonperfusion in nonproliferative diabetic retinopathy


El-Minia University Hospital, Faculty of Medicine, El-Minia University, El-Minia, Egypt

Date of Submission08-Sep-2015
Date of Acceptance22-Dec-2015
Date of Web Publication21-Oct-2016

Correspondence Address:
Heba R AttaAllah
El-Minia University Hospital, Faculty of Medicine, El-Minia University, El-Minia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2090-0686.192748

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  Abstract 

Aim
The aim of this study was to correlate the visual field changes in the central macular area with the areas of capillary nonperfusion seen in fluorescein angiogram in patients with nonproliferative diabetic retinopathy (NPDR).
Patients and methods
This study included 40 eyes of 32 patients with NPDR attending the Ophthalmic Outpatient Clinic of El-Minia University Hospital during the period from January 2012 to July 2013. All patients were subjected to automated perimetry using a Topcon perimeter. A full-threshold strategy was applied for the central 10° field (program 10–2) fluorescein angiography using the IMAGE Net 2000 fundus camera.
Results
This study included 40 eyes of 32 patients between 50 and 70 years of age with a mean of 59.3 ± 7.6 years. Of them, there were 12 (37.5%) male and 20 (62.5%) female patients. All patients were noninsulin-dependent diabetic patients with a mean duration of 16.6 ± 5.4 years; 20 (62.5%) patients were hypertensive and 12 (37.5%) were normotensive. Twenty eyes had a rate of 0 dB corresponding to areas of capillary nonperfusion. Sixteen eyes showed a rate of 0 dB less than the areas of capillary nonperfusion. Four eyes showed relatively good retinal sensitivity (rate of 0 dB = 0) despite the presence of definite areas of capillary nonperfusion. The mean sensitivity in these areas ranged between 10.38 ± 1.47 and 12.91 ± 1.43 dB.
Conclusion
There is a significant correspondence between macular capillary nonperfusion and central field sensitivity in patients with NPDR.

Keywords: capillary dropout, macular ischemia, macular sensitivity


How to cite this article:
Hammouda LM, Eid AM, AttaAllah HR, Ali ES. Macular sensitivity in areas of capillary nonperfusion in nonproliferative diabetic retinopathy. J Egypt Ophthalmol Soc 2016;109:26-31

How to cite this URL:
Hammouda LM, Eid AM, AttaAllah HR, Ali ES. Macular sensitivity in areas of capillary nonperfusion in nonproliferative diabetic retinopathy. J Egypt Ophthalmol Soc [serial online] 2016 [cited 2022 Dec 1];109:26-31. Available from: http://www.jeos.eg.net/text.asp?2016/109/1/26/192748


  Introduction Top


Diabetic retinopathy (DR) is the most common microvascular complication of diabetes and remains one of the leading causes of blindness worldwide among adults aged 20–74 years. The two most important visual complications of DR are diabetic macular edema and proliferative diabetic retinopathy (PDR). The prevalence of DR increases with the duration of diabetes. Nearly all people with type 1 diabetes and more than 60% of those with type 2 have retinopathy after 20 years [1].

The diagnostic problem of diabetic maculopathy consists in detecting very early morphologic and functional deficits related to later visual outcome. The established assessment of visual acuity does not have a high predictive value in the early stages, because acuity remains stable until ∼55% of all neuroretinal channels are affected [2]. Morphologic changes assessed by means of fluorescein angiography, effective for detecting and quantifying capillary changes, are not reflected in visual acuity loss until the disease is well progressed [3].

Visual field changes are commonly associated with DR. Most studies have focused on proliferative and severe nonproliferative stages when fundus alterations are clearly visible with ophthalmoscopy or fluorescein angiography. Thus, deep and large scotomas are associated with larger nonperfusion areas [3] and small scotomas with cotton–wool spots [4].


  Aim Top


The aim of this study was to correlate the visual field changes in the central macular area with the areas of capillary nonperfusion seen in fluorescein angiogram in patients with nonproliferative diabetic retinopathy (NPDR).


  Patients and methods Top


This prospective study included 40 eyes of 32 patients with NPDR attending the Ophthalmology Outpatient Clinic of El-Minia University Hospital during the period from January 2012 to July 2013. Their ages ranged between 50 and 70 years. There were 12 male and 20 female patients.

Inclusion criteria

Inclusion criteria were as follows:

  1. Noninsulin-dependent diabetic patients (20 were hypertensive, and 12 were normotensive).
  2. Visual acuity of more than 3/60.


Exclusion criteria

Exclusion criteria were as follows:

  1. Having glaucoma.
  2. PDR.
  3. Previous retinal laser photocoagulation.
  4. Previous intraocular surgery.
  5. Presence of visually significant media opacities.


All patients were subjected to the following:

  1. Careful history taking: demographic data (name, age, and sex), type and duration of diabetes, and associated medical conditions (hypertension).
  2. Ophthalmologic examination:
  3. Best-corrected visual acuity assessment using a Landolt-C chart.
  4. Intraocular pressure measurement using an applanation tonometer.
  5. Anterior segment examination using a slit lamp biomicroscope.
  6. Refraction assessment using an autorefractometer.
  7. Fundus examination using indirect ophthalmoscope and slit lamp biomicroscope with Volk 90 D lens.


Other investigations:

(8a) Visual field testing using a Topcon perimeter (Topcon SBP 3000, version 1.76; Topcon Corporation, Japan). Stimulus size was Goldmann III, white. The background measured 10 cd/m2 (31.5 asb). A full-threshold strategy was applied for the central 10° field (program 10–2). Blind spot monitoring technique was Heijl–Krakau visual field analysis. The number of patients with visual field defects was obtained by observing areas of absolute and relative loss of sensitivity on the gray tone format and pattern deviation of the printout. The statistical program of the device provides global indices, which compare the threshold visual field results with those of age-controlled normal.

Mean defect (MD): It is the mean elevation or depression of the overall field compared with the age-matched normal reference field.

Loss variance (LV): It shows how homogenous the entire visual field is (the shape of the patient's hill of vision) and whether individual areas clearly deviate from the rest of the results. No major in homogenicity is present if this value is below 25. The value would then be viewed as normal.

The number of patients who had abnormal fields based on the values of the MD and LV was recorded.

(8b) Fluorescein angiography: The reasons for performing FA, the procedure, and its possible side effects were explained to the patient. The IMAGE Net 2000 fundus camera (Topcon Corporation) was used. The pupils were dilated with 1% tropicamide and 5% phenylephrine at least 30 min before the procedure, and intravenous access was secured.

Color fundus photograph was taken before angiography. The angiography was started with an intravenous bolus administration of 5 ml sodium fluorescein (500 mg/5 ml). A standard image of 50° was used; additional 35° and 20° (high magnification) were used.

Angiography is concluded with the last exposures being taken 5 min after the initial injection (late phase). Areas of capillary dropout are defined in the angiogram as areas of hypofluorescence, indicating reduced levels of tissue perfusion.

Identification of the correlation between capillary nonperfusion and visual field defects

The visual fields of the 40 eyes were compared with their fluorescein fundus angiograms to assess the correlation between visual field loss and areas of capillary nonperfusion. The fluorescein angiograms were inverted along the horizontal axis and superimposed onto the numeric format of the field test result so that the fovea corresponded with the fixation point.


  Results Top


This study included 40 eyes of 32 patients attending the Ophthalmic Outpatient Clinic of El-Minia University Hospital during the period from January 2012 to July 2013. The patients’ ages ranged between 50 and 70 years, with a mean of 59.3 ± 7.6 years; there were 12 (37.5%) male and 20 (62.5%) female patients. All were noninsulin-dependent diabetic patients, with a mean duration of 16.6 ± 5.4 years; 20 (62.5%) were hypertensive and 12 (37.5%) were normotensive.

The study population was grouped according the international clinical DR severity scale into two groups:

  1. Twenty-four (60%) eyes with moderate NPDR.
  2. Sixteen (40%) eyes with severe NPDR.


There is no significant difference (P > 0.05) among the two types of retinopathy as regards age, duration of DM, and the presence of hypertension ([Table 1]).
Table 1: Comparison between the two groups according to the clinical data

Click here to view


In [Table 2], 20 eyes had a rate of 0 dB corresponding to areas of capillary nonperfusion – that is, the mean sensitivity within the areas of capillary nonperfusion was 0. In 16 eyes the rate of 0 dB was less than that in the areas of capillary nonperfusion; the mean sensitivity within these areas ranged between 1.5 ± 0.7 and 6.5 ± 2.16 dB. Four eyes showed relatively good retinal sensitivity (rate of 0 dB = 0) despite the presence of definite areas of capillary nonperfusion; the mean sensitivity in these areas ranged between 10.38 ± 1.47 and 12.91 ± 1.43 dB.
Table 2: The rate of 0 dB (no response) within areas of capillary nonperfusion

Click here to view


In [Table 3], the correlation between the mean sensitivity within areas of capillary nonperfusion with the age, duration of DM, and presence of hypertension was statistically nonsignificant.
Table 3: Correlation between the mean sensitivity within areas of capillary nonperfusion as regards the clinical data

Click here to view


[Table 4] shows comparison between the MD and LV of the two groups. The relation of the severity of depression in retinal sensitivity to the type of retinopathy is not significantly different (P > 0.05). However, as regards the P value of LV there was a significant difference, indicating a correlation between the loss of homogenicity of the visual field and the severity of retinopathy. The loss of homogenicity of the visual field was more severe in patients with severe NPDR ([Figure 1] and [Figure 2]).
Table 4: Comparison between the two groups according to mean defect and loss variance

Click here to view
Figure 1: FA of the right eye showing areas of capillary nonperfusion (white arrow) in the macular area.

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Figure 2: FA of the same patient after superimposition of the numerical display on it.

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  Discussion Top


In the early stages of DR, visual acuity is not sufficiently sensitive to provide clinical information about the impact of altered retinal function [5]. Frisén and Frisén [6] found that visual acuity remains normal until ∼55% of the neuroretinal channels are affected. The loss of macular function may be unrelated to the stage of retinopathy and remains the most common sight-threatening complication of DR [7]. In DR patients with normal visual acuity some studies have shown that contrast sensitivity was significantly reduced [8]. Early color vision defects were reported, in other studies, before DR occurs [9],[10]. Furthermore, a high spatial frequency loss of contrast sensitivity points to an early involvement of parvocellular cells or cone-specific alterations in the diabetic disease course [11].

Defects in the visual fields reflect the structural abnormalities in the ocular and neural mechanisms of vision. In diabetes, the visual field defects are rarely considered to be the major feature of background and preproliferative retinopathy [12].

The aim of this work was to correlate the visual field changes in the central macular area with the areas of capillary nonperfusion seen in fluorescein angiogram in patients with NPDR, as central field defects reflect early changes in the macular area.

In this study, all 40 eyes showed areas of capillary nonperfusion in the macular area demonstrated on fluorescein angiography. All eyes had obvious areas of reduced retinal sensitivity as shown by the gray tone printout and the corrected deviation map within the areas of capillary nonperfusion. This is in agreement with the findings of Unoki et al. [13], although they used microperimetry to assess the retinal sensitivity. A total of 20 (50%) eyes had a rate of 0 dB corresponding to areas of capillary nonperfusion – that is, the mean sensitivity within the areas of capillary nonperfusion was 0. In 16 (40%) eyes, the rate of 0 dB was less than that in the areas of capillary nonperfusion; the mean sensitivity within these areas ranged between 1.5 ± 0.7 and 6.5 ± 2.16 dB. Four (10%) eyes in this study showed relatively good retinal sensitivity (rate of 0 dB = 0) despite the presence of definite areas of capillary nonperfusion; the mean sensitivity in these areas ranged between 10.38 ± 1.47 and 12.91 ± 1.43 dB ([Table 2]). There was no significant correlation between the mean sensitivity within areas of capillary nonperfusion with the age, duration of DM, and presence of hypertension ([Table 3]). This is also in agreement with the findings of Unoki et al. [13].

These findings suggest a significant correspondence between macular capillary nonperfusion and central field sensitivity in DR. On the basis of the results of the automated perimetry, light sensitivity was reduced markedly in the area of capillary nonperfusion secondary to moderate and severe NPDR. This is in agreement with the findings of Unoki et al. [13] and Remky et al. [7].

The inner retinal layers may be particularly at risk for hypoxic insult because they are supplied with oxygen from the retinal vasculature, which is relatively sparse, compared with the choroidal circulation, which supplies most of the outer retina [14]. In addition, the temporal part of the macula is characterized by a lower density of capillaries, and thus is the first to become ischemic [15]. Bek [16] reported the histopathologic features of capillary-free areas in DR. In his study, he showed a homogenous eosinophil substance accumulated between the photoreceptor outer segments and the RPE corresponding to the areas with inner retinal changes. Accordingly, the reduction of light sensitivity in areas of capillary nonperfusion may be the result of a malfunction of cells of the inner and outer retina [16].

Four eyes in our study maintained relatively good retinal sensitivity (mild depression of retinal sensitivity) despite reduced capillary perfusion. The mean sensitivity in these areas ranged between 10.38 ± 1.47 and 12.91 ± 1.43. Their ages ranged between 50 and 57 years. They were normotensive with severe DR. Chee and Flanagan [3] also reported in their study a relatively young patient who was a 43-year-old female with good retinal sensitivity despite reduced capillary perfusion. They explained that younger patients had significantly less severe visual field loss. The reasons are not clear. Perhaps younger neurons are more resistant to hypoxia and metabolic imbalance, or the presence of a healthy choroid, not yet affected by atherosclerotic vascular disease, contributes to the maintenance of good retinal sensitivity [3].

The effect of age on the macular sensitivity was not significant; there is inverse fair relationship between the MD and age of the patients, with moderate NPDR (i.e. MD value is greater in young patients); however, there was no association between MD and the age in patients with severe NPDR. This finding is in contrary to that of Chee and Flanagan [3], who found that the visual field defects were more severe in older patients. This difference may be referred to the wider examination area, as they used 30–2 test strategy, or the patient criteria, as their study included preproliferative and PDR patients [3].

As regards the homogenicity of the visual field loss as indicated by LV P value, it was found that there was a significant difference between LV and the type of retinopathy, and there was a strong association between the type of retinopathy and LV. This means that the loss of homogenicity of the visual field defect was more severe in patients with severe NPDR, as LV value increases in severe NPDR patients. This is in agreement with the findings of Henricsson and Heijl [17], who investigated different stages of DR using the Humphrey perimeter, and found no evidence of field loss in eyes with mild retinopathy, with defects only becoming evident in eyes with more advance retinopathy. Moreover, in a study by Ismail [18], visual field defects were more related to the severity of the retinopathy rather than the duration of diabetes. However, Jeddi et al. [19] found some evidence of visual field defects in their early diabetic groups (35% of their cases) compared with matched control groups.

As regards the severity of depression in retinal sensitivity in correlation with the severity of the retinopathy, it was not statistically significant ([Table 4]); however, it was found to be significant in the study by Chee and Flanagan [3].

In conclusion, macular sensitivity is reduced in nonproliferative diabetic patients relative to their age-matched normative normal. The homogeneity of the visual field defects is reduced by the severity of retinopathy. We focused on the macular area, as the loss of macular function may be unrelated to the stage of retinopathy, and it is the most significant vision-threatening complication of DR.

More recent investigative tools, such as multifocal ERG, which is an objective functional tool to test for macular dysfunction in cases of ischemic DR, may add further information about macular sensitivity in such cases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Fong DS, Aiello L, Gardner TW, King GL, Blankenship G, Cavallerano JD et al. American Diabetes Association. Diabetic retinopathy. Diabetes Care 2003; 26:226–229.  Back to cited text no. 1
    
2.
Angiography of macular disease. In: Fernando, J.A., editor. Retinal angiography and optical coherence tomography. Vol. 4.; 2009. pp. 61-105.  Back to cited text no. 2
    
3.
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4.
Bek T, Lund-Andersen H. Cotton–wool spots and retinal light sensitivity in diabetic retinopathy. Br J Ophthalmol 1991; 75:13–17.  Back to cited text no. 4
    
5.
Regan D, Neima D. Low-contrast letter charts in early diabetic retinopathy, ocular hypertension, glaucoma, and Parkinson's disease. Br J Ophthalmol 1984; 68:885–889.  Back to cited text no. 5
    
6.
Frisén L, Frisén M. A simple relationship between the probability distribution of visual acuity and the density of retinal output channels. Acta Ophthalmol (Copenh) 1976; 54:437–444.  Back to cited text no. 6
    
7.
Remky A, Arend O, Hendricks S. Short-wavelength automated perimetry and capillary density in early diabetic maculopathy. Invest Ophthalmol Vis Sci 2000; 41:274–281.  Back to cited text no. 7
    
8.
Arend O, Remky A, Evans DW, Stüber R, Harris A. Contrast sensitivity loss is coupled with capillary drop out in diabetic patients with unaffected visual acuity. Invest Ophthalmol Vis Sci 1997; 38:1819–1824.  Back to cited text no. 8
    
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Green FD, Ghafour IM, Allan D, Barrie T, McClure E, Foulds WS. Color vision of diabetics. Br J Ophthalmol 1985; 69:533–536.  Back to cited text no. 9
    
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Bresnick GH, Condit RS, Palta M, Korth K, Groo A, Syrjala S. Association of hue discrimination loss and diabetic retinopathy. Arch Ophthalmol 1985; 103:1317–1324.  Back to cited text no. 10
    
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Harris A, Arend O, Danis RP, Evans D, Wolf S, Martin BJ. Hyperoxia improves contrast sensitivity in early diabetic retinopathy. Br J Ophthalmol 1996; 80:209–213.  Back to cited text no. 11
    
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Trick GL, Trick LR, Kilo C. Visual field defects in patients with insulin-dependent and noninsulin-dependent diabetes. Ophthalmology 1990; 97:475–482.  Back to cited text no. 12
    
13.
Unoki N, Nishijima K, Sakamoto A, Kita M, Watanabe D, Hangai M et al. Retinal sensitivity loss and structural disturbance in areas of capillary nonperfusion of eyes with diabetic retinopathy. Am J Ophthalmol 2007; 144:755–760.  Back to cited text no. 13
    
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Yu DY, Cringle SJ, Su EN. Intraretinal oxygen distribution in the monkey retina and the response to systemic hyperoxia. Invest Ophthalmol Vis Sci 2005; 46:4728–4733.  Back to cited text no. 14
    
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Wolf S, Arend O, Schulte K, Ittel TH, Reim M. Quantification of retinal capillary density and flow velocity in patients with essential hypertension. Hypertension 1994; 23:464–467.  Back to cited text no. 15
    
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Bek T. Transretinal histopathological changes in capillary-free areas of diabetic retinopathy. Acta Ophthalmol (Copenh) 1994; 72:409–415.  Back to cited text no. 16
    
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Henricsson M, Heijl A. Visual fields at different stages of diabetic retinopathy. Acta Ophthalmol (Copenh) 1994; 72:560–569.  Back to cited text no. 17
    
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Ismail GM. Visual field deficit in diabetes mellitus in presence of no or minimal diabetic retinopathy. Sudanese J Ophthalmol 2013; 5:49–53.  Back to cited text no. 18
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Jeddi A, Ben Osman N, Daghfous F, Kaoueche M, Baccar M, Gaigi S. Ayed S Methods for screening and surveillance of diabetic retinopathy. J Fr Ophtalmol 1994; 17:769–773.  Back to cited text no. 19
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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