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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 21  |  Issue : 2  |  Page : 75-81

Evaluation of ocular surface in type 2 diabetic patients


1 Ophthalmology Resident, Alexandria General Eye Hospital, Alexandria, Egypt
2 Department of Ophthalmology, Faculty of Medicine, Alexandria University, Alexandria, Egypt

Date of Submission10-Feb-2020
Date of Decision11-Mar-2020
Date of Acceptance23-Mar-2020
Date of Web Publication26-Jun-2020

Correspondence Address:
MD Reham S Badr
63 Hoda El Eslam Street, Behind Khalifa Bakery, Sidi Bishr, Alexandria 21624
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/DJO.DJO_12_20

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  Abstract 


Purpose The aim of this study was to evaluate the tear film and the changes in ocular surface in type 2 diabetic patients.
Patients and methods This is a prospective, cross-sectional, observational, hospital-based study of 100 participants (200 eyes). They included 50 diabetic patients (100 eyes) and 50 healthy controls (100 eyes), of either sex above 40 years old, who were evaluated at Alexandria General Eye Hospital, Alexandria, Egypt. History was taken from all participants including ocular surface disease index questionnaire. All participants underwent full ophthalmological examination, Schirmer’s test, tear film breakup time, corneal staining, and rose Bengal staining tests.
Results When compared with the healthy controls, diabetic patients showed significantly reduced Schirmer’s test, tear breakup time measurements, and higher grades of corneal and rose Bengal staining (P<0.001). Ocular surface disease index was severe in 70% of diabetics. There was a significant difference between the two groups regarding the dry eye severity grade according to Dry Eye Workshop, as most of diabetic patients were grades 3 and 2 (37 and 53%, respectively), whereas 64% of the controls were grade 1.
Conclusion Tear film abnormality was a significant feature of diabetic ocular surface disease, which suggests that diabetic patients are more prone to experience dry eye than normal participants. Therefore, all diabetic patients should undergo routine early examination and follow-up of tear function and ocular surface parameters.

Keywords: cornea, diabetes, eye


How to cite this article:
Badr RS, Fadel AM, Allam IY, Osman IM. Evaluation of ocular surface in type 2 diabetic patients. Delta J Ophthalmol 2020;21:75-81

How to cite this URL:
Badr RS, Fadel AM, Allam IY, Osman IM. Evaluation of ocular surface in type 2 diabetic patients. Delta J Ophthalmol [serial online] 2020 [cited 2020 Sep 22];21:75-81. Available from: http://www.djo.eg.net/text.asp?2020/21/2/75/287459




  Introduction Top


Currently, an estimated 347 million people in the world have diabetes mellitus (DM), making it one of the most common medical conditions worldwide [1]. Diabetes has received widespread attention, as it causes life-threatening or debilitating complications in the heart, kidney, brain, and eye [2]. In the eye, diabetic retinopathy, cataract, glaucoma, keratopathy, chronic dry eye, and refractive abnormalities are the diseases associated with diabetes [3].

Besides the disorders in the retina, the incidence of corneal abnormalities is also high in DM. Literature has shown that diabetics have an increased risk of developing corneal epithelial fragility and defects, decreased corneal sensitivity and thickness, abnormal wound healing, and increased susceptibility to infected corneal ulceration [4],[5].

In this study, the tear film and ocular surface parameters were evaluated in type 2 diabetic patients compared with controls to better understand the effect of type 2 DM on the ocular surface.


  Patients and methods Top


This is a prospective, cross-sectional, observational, hospital-based study that examined 100 participants (200 eyes). They included 50 diabetic patients (100 eyes) and 50 healthy controls (100 eyes), of either sex above 40 years old who presented to the Outpatient Eye Clinic of Alexandria General Eye Hospital, Alexandria, Egypt, from May 2018 to May 2019. The study was approved by the Local Ethical Committee of the Faculty of Medicine, Alexandria University. All participants signed a written informed consent to participate in the study and for publication of data before enrollment in the study.

The study included patients diagnosed with DM type 2 of more than 5 years of duration, who were above 40 years old.

Patients with ocular infections, lid deformity or abnormal lid movement disorders, refractive surgery within 1 year of the study visit, current pregnancy or lactation, abnormal nasolacrimal drainage, corneal opacity, or systemic diseases known to be associated with dry eye such as sarcoidosis, rheumatoid arthritis, or Sjogren’s syndrome were excluded from the study.

Data of all patients including a questionnaire, sex, age, duration of diabetes, as well as medical and ocular disease history were collected.

Ocular surface disease index [6]

A wide variety of questionnaires are available for the evaluation of dry eye disease, such as ocular surface disease index (OSDI), National Eye Institute Visual Function Questionnaire (NEIVFQ-25), and McMonnies Dry Eye Questionnaire [6]. The OSDI questionnaire, developed by the Outcomes Research Group at Allergan Inc. (Irvine, California, USA), is a useful tool for dry eye disease evaluation because of its simplicity and ease of use, and therefore, it was used in this study. It is a 12-item scoring survey, in which the patient rates his or her own ocular symptoms induced by environmental factors over the preceding 2–4 weeks. Answers are scored on a scale from 0 to 4; the total score can range from 0 to 100, with higher scores representing greater disability. The OSDI has an overall score and three subscale scores [ocular symptoms (three items), vision-related function (six items), and environmental triggers (three items)]. Each OSDI item is scored on a Likert-type scale ranging from 0 to 4 points, where 0 indicates none of the time and 4 indicates all of the time. On the basis of their OSDI scores, patients can be categorized as having a normal ocular surface (0–12 points) or as having mild (13–22 points), moderate (23–32 points), or severe (33–100 points) ocular surface disease ([Figure 1]).
Figure 1 Ocular surface disease index (OSDI) [6].

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A complete ocular examination was carried out in the following sequence:

All participants got full ophthalmological examination of both eyes. External ocular examination was done. The lids were examined for the presence of any anatomical abnormalities interfering with normal spread of the tear film. Slit-lamp biomicroscopy was performed, and the presence of mucus strands in the tear film and corneal filaments was noted. Lid margins were examined for irregularity or thickening. Meibomian orifices were examined for pouting, presence of foam, secretion, and plugging. The tarsal conjunctiva was examined for the presence of papillae. This was followed by the following:

Tear film evaluation: which was done in the following order:
  • Tear meniscus height (TMH) was recorded as normal, which is 0.46±0.17 mm, or low, which is 0.24±0.09 mm (under slit lamp, thin beam).
  • Precorneal tear film was observed for presence of debris (mucous/oil droplets/debris).


Tear breakup time measurement

Moistened with nonpreservative saline, fluorescein strips (Omni Strips Fluro, Ophthalmic Strips, Omni Unlimited, Gujarat, India) were introduced into the conjunctival sac with minimal stimulation, undetected by the patient. The individuals were then instructed to blink several times for a few seconds to ensure adequate mixing of fluorescein. The tear film was examined with a broad beam and a cobalt blue filter. The interval between the last complete blink and the appearance of the first corneal black spot or line in the stained tear film was measured using a stopwatch. A tear film breakup time (TBUT) value more than 10 s (s) was considered normal, a value of 8–10 s was considered mild dryness, a value of 5–7 s was considered moderate dryness, and a value less than 5 s was considered severe dryness [7],[8].

Fluorescein staining of the cornea: using fluorescein strips moistened with nonpreservative saline, was graded from 0 to 3 [9]:
  1. 0: no staining of corneal epithelial surface.
  2. 1: mild staining occupying less than 1/3 of corneal epithelial surface.
  3. 2: moderate staining occupying less than 1/2 of corneal epithelial surface.
  4. 3: severe staining occupying more than 1/2 of the corneal epithelial surface.


Schirmer’s test: without topical anesthesia (total tear secretion) and Schirmer’s test with topical anesthesia (basal tear secretion) using Opstrip filter paper (Schirmer’s tear test strips, Ophtechnics Unlimited, Haryana, India) [7],[8].
  1. Dry eye severity was classified into mild, moderate, severe, and very severe (level 1–4) according to Dry Eye Workshop (DEWS). Dry eye grading system was as follows ([Table 1]).
    Table 1 Dry eye severity grading system according to Dry Eye Workshop

    Click here to view


Rose Bengal staining (RBS) test: was done using saline-moistened rose Bengal strips (Optiros, Ophtechnics Unlimited, Parwanoo, Himachal Pradesh, India) placed in the lower fornix. The staining of nasal and temporal conjunctiva was graded from 0 to 3 [10]. Grade 0 referred to no staining, grade 1 to the staining of few points, grade 2 to a scattered pattern, and grade 3 referred to staining of confluent areas of the ocular surface. If the sum of these staining scores was more than or equal to 3, it was considered abnormal.

The sequence of these tests was maintained so that each test was not affecting the following one.

Statistical analysis

Data were fed to the computer and analyzed using IBM SPSS software package, version 20.0 (IBM Corp., Armonk, New York, USA). Qualitative data were described using number and percent. The Kolmogorov–Smirnov test was used to verify the normality of distribution. Quantitative data were described using range (minimum and maximum), mean, SD, and median. Tests utilized for class differences included the χ2-test for categorical variables and the Student t test for continuous variables. Significance of the obtained results was judged at the 5% level.


  Results Top


This study was conducted on 100 participants (200 eyes): 50 diabetic patients (100 eyes) and 50 healthy controls (100 eyes). The mean age was 53.50±5.37 years in diabetics and 56.48±4.63 years in the control group, with a female predominance of 68% in the diabetic group and 72% in the healthy controls. There was a statistically significant difference between nondiabetics and diabetics regarding age (P=0.004), whereas there was no statistically significant difference regarding sex (P<1.000, [Table 2]).
Table 2 Comparison between the two studied groups according to demographic data

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There was a significant increase in OSDI score in diabetic patients compared with the control group, as it ranged from 33 to 100, denoting a severe ocular surface disease, in 70% of the diabetic patients ([Table 3]).
Table 3 Comparison between the two studied groups according to ocular surface disease index questionnaire

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The TBUT values of diabetics were significantly lower than those of the nondiabetics (P<0.001). In diabetics, the mean TBUT was 5.0±2.17 s, whereas in the nondiabetics, it was 7.71±3.48 s. There was a significant decrease in the TMH in diabetic patients compared with nondiabetics (P<0.001). In diabetics, the mean TMH was 0.25±0.10 mm, whereas in nondiabetics, it was 0.40±0.15 mm ([Table 4]).
Table 4 Compassion between the two studied groups according to tear breakup time and tear meniscus height

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Schirmer’s test values without and with anesthesia were significantly lower in diabetics compared with nondiabetics (P<0.001). In diabetics, the mean Schirmer’s test values without and with anesthesia were 6.21±3.33 and 8.96±3.80 mm, respectively, whereas in nondiabetics, it was 12.42±5.36 and 14.73±5.97 mm, respectively ([Table 5]).
Table 5 Comparison between the two studied groups according to Schirmer’s test without and with anesthesia

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Compared with the nondiabetic group, the positive staining rate of rose Bengal in the diabetic group was increased significantly (P<0.001), as 75% of diabetics were stained positively with rose Bengal, whereas only 33% of nondiabetics stained positively with rose Bengal ([Table 6]).
Table 6 Comparison between the two studied groups according to rose Bengal staining

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There was a significant difference between diabetics and nondiabetics regarding fluorescein staining grade (P<0.001). In nondiabetics, 83% had grade 0 fluorescein staining, whereas in diabetics, 51% had grade 1 fluorescein staining ([Table 7]).
Table 7 Comparison between the two studied groups according to fluorescein staining grade

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In addition, there was a significant difference between the two groups regarding dry eye severity according to DEWS, as dry eye severity was grades 2 and 3 in 53 and 37% of the diabetics, respectively, but was only grade 1 in 64% of the controls ([Table 8]).
Table 8 Comparison between the two studied groups according to dry eye severity grade according to Dry Eye Workshop

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  Discussion Top


Several clinical and experimental studies have reported structural, metabolic, and functional abnormalities in the conjunctiva and cornea of patients with DM and have suggested that these abnormalities may be responsible for the corneal complications of diabetes.

In the current study, the Schirmer’s test, TMH, and TBUT values in diabetics were significantly lower than those of nondiabetics. RBS was worse in the diabetic patients compared with the nondiabetics. In addition, OSDI score and dry eye severity grading, according to DEWS, of the diabetics was statistically higher than those of the nondiabetics.

In the current study, there was a statistically significant difference between nondiabetics and diabetics regarding age, whereas there was no statistically significant difference regarding sex. Unlike the present study, Yoon et al. [11] showed that there were no significant differences in age or sex between the diabetic and normal control groups. Moreover, De Cilla et al. [12] showed that the mean age and sex were not significantly different in the diabetic and control groups. The differences between the current study and these studies may be owing to the difference in the number of included patients in this study.

In the current study, there was a significant increase in OSDI scores in diabetic patients compared with controls, with severe ocular surface disease (33–100 points) in 70% of diabetic patients. Consistent with these findings, DeMill et al. [13] showed that OSDI scores tended to be lower in controls than in the groups with DM. The mechanisms leading to ocular surface disease in diabetics are complex but are related to three main factors: chronic hyperglycemia and its sequelae, corneal nerve damage, and impairment of insulin action [14].

In the present study, the TBUT was significantly lower in the diabetic group (5.0±2.17 s) than in the control group (7.71±3.48 s). In addition, the TMH was significantly lower in the diabetic group (0.25±0.10 mm) than the control group (0.40±0.15 mm). Similarly, Yoon et al. [11] showed that the TBUT was significantly shorter in the diabetic group (7.82±2.12 s) than in the control group (10.95±1.56 s). The total and basal tear secretions were 12.88±5.06 and 6.95±3.76 mm, respectively, in the diabetic group, and 19.26±3.06 and 11.22±2.10 mm, respectively, in the control group. The differences between the two groups were statistically significant [11]. Similarly, in the current study, there was a highly significant decrease in the value of Schirmer’s test with (basal tear secretion) and without anaesthesia (total tear secretion), and their mean values in diabetics were 6.21±3.33 and 8.96±3.80 mm, respectively, compared with 12.42±5.36 and 14.73±5.97 mm, respectively, in nondiabetics. In agreement with our results, Gao et al. [15] showed that there was a highly significant difference among the groups and also between the nonproliferative diabetic retinopathy (NPDR) or the proliferative diabetic retinopathy (PDR) and the control group. The percentage of the patients with Schirmer’s I test value less than 5 mm was 8.82% (3/34 eyes) in the NPDR group, 15% (6/40 eyes) in the PDR group, and only 2.78% (1/36 eyes) in the control group. In addition, our findings were similar to Akinci et al. [16] who found that diabetics had a lower TBUT and Schirmer’s test values than nondiabetics. Findings from the current study are essentially in accordance with the majority of that in literature that the diabetics have lower Schirmer’s test and TBUT values than nondiabetics. This could be owing to decreased corneal and conjunctival sensitivity in diabetics and owing to damage of the microvasculature of the lacrimal gland leading to its impaired functioning.

In the current study, there was a significant increase in RBS in diabetics compared to nondiabetics, being positively stained in 75% of diabetics’ eyes. Yu et al. [17] showed that the positive RBS rate in the diabetic group was increased significantly compared to controls.

In the current study, there was a significant difference between the two groups regarding fluorescing staining grade, as in the nondiabetics, 83% were grade 0 (no staining) but 51% of diabetics were grade 1 (<1/3 of corneal epithelial surface stained). Gao et al. [15] showed that the corneal staining score in the PDR group was significantly higher than that in the control group and the NPDR group, and the staining score in all diabetic patients was positively correlated with the disease duration. These results suggest that the damage to the intactness of corneal epithelia may start in diabetic patients without retinopathy and that the damage becomes more severe as diabetes progresses.


  Conclusion Top


Type 2 diabetics are predisposed to various changes in the ocular surface, which should be noted at an early stage and treated appropriately to prevent more severe ocular complications.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Jones LT. The lacrimal secretory system and its treatment. Am J Ophthalmol 1966; 62:47–60.  Back to cited text no. 8
    
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DeMill DL, Hussain M, Pop-Busui R, Shtein RM. Ocular surface disease in patients with diabetic peripheral neuropathy. Br J Ophthalmol 2016; 100:924–928.  Back to cited text no. 13
    
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Juthani V, Dupps WJ. Ocular surface disease in diabetes. In: Sing R, ed. Managing diabetic eye disease in clinical practice. 1st ed. Switzerland: Adis Cham 2015. 71–80  Back to cited text no. 14
    
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

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