Evaluation of choroidal thickness in patients with ulcerative colitis

Ali Kurt; Raşit Kılıc; Bilal Ergul; Caglar Oktem

doi:10.4103/1858-540X.198539

ORIGINAL ARTICLE

Year : 2016 | Volume : 8 | Issue : 2 | Page : 51-55

Evaluation of choroidal thickness in patients with ulcerative colitis

Ali Kurt¹, Raşit Kılıc¹, Bilal Ergul², Caglar Oktem¹
¹ Department of Ophthalmology, Ahi Evran University Medical School, Training and Research Hospital, Kırşehir, Turkey
² Department of Gastroenterology, Ahi Evran University Medical School, Training and Research Hospital, Kırşehir, Turkey

Date of Web Publication

17-Jan-2017

Correspondence Address:
Ali Kurt
Department of Ophthalmology, Ahi Evran University Medical School, Training and Research Hospital, Kırşehir
Turkey

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/1858-540X.198539

Abstract

Purpose: To evaluate the effect of ulcerative colitis (UC) on the choroid by measuring the choroidal thickness (CT) and also to determine any difference between CT in the Montreal classification groups. Materials and Methods: We included 36 eyes of 36 UC patients and 36 controls in the study. The UC patients were classified as ulcerative proctitis, left-sided (distal) UC, and extensive UC (pancolitis) according to the Montreal classification. CT was measured using enhanced depth imaging optic coherence tomography at the foveal center and at 500 μm, 1000 μm, and 1500 μm from the foveal center for each eye. Results: CT was significantly thinner in patients with UC than controls at 500 μm temporal to the fovea (P = 0.026), at 500 μm nasal to the fovea (P = 0.019), at 1000 μm nasal to the fovea (P = 0.042), and at 1500 μm nasal to the fovea (P = 0.013). There was no statistically significant difference between these three groups regarding the CT value (P > 0.05). Conclusions: Perifoveal CT was significantly thinner in patients with UC than in healthy controls. There was no statistically significant difference between these three groups (ulcerative proctitis, left-sided UC, and extensive UC) regarding the CT value.

Keywords: Choroidal thickness, enhanced depth imaging, Montreal classification, optical coherence tomography, ulcerative colitis

How to cite this article:
Kurt A, Kılıc R, Ergul B, Oktem C. Evaluation of choroidal thickness in patients with ulcerative colitis. Sudanese J Ophthalmol 2016;8:51-5

How to cite this URL:
Kurt A, Kılıc R, Ergul B, Oktem C. Evaluation of choroidal thickness in patients with ulcerative colitis. Sudanese J Ophthalmol [serial online] 2016 [cited 2023 Jun 2];8:51-5. Available from: https://www.sjopthal.net/text.asp?2016/8/2/51/198539

Introduction

Ulcerative colitis (UC) is a chronic inflammatory bowel disease characterized by diffuse inflammation of the mucosa of the colon and rectum. UC can occur at any age but is most commonly diagnosed in late adolescence or early adulthood. ^[1],[2] The intestinal tract is not the only organ involved, and UC can also involve other organs such as the eyes, skin, joints, liver and biliary tracts, kidneys, lungs, and the vascular system. ^[3] Extraintestinal manifestations (EIMs) can be found in 15%-20% of UC patients. ^[4]

Ocular complications occur in <10% of UC patients and include anterior uveitis, episcleritis, and conjunctivitis. ^[5],[6],[7] Anterior uveitis is the most common ocular complication. ^[6] Most UC patients are diagnosed prior to the development of ophthalmic complications, but ocular disorders can be the initial manifestation. ^[8]

Complications such as periphlebitis and retinal venous and arterial system occlusion in UC indicate a potential for changes in the choroidal vasculature as a result of developing ischemia. ^{[9],[10],[11]}

Our aim was to evaluate the effect of UC on the choroid by measuring the choroidal thickness (CT) and also to determine any difference between CT in the Montreal classification groups.

Materials and Methods

We compared CT values in UC patients and healthy control participants referred to the Gastroenterology Clinic at Ahi Evran University Training and Research Hospital in this cross-sectional study. We included 36 eyes of 36 patients with UC and 36 controls without UC in the study. The left eye was evaluated in all participants. Written consent was obtained from all participants after they were informed about the study. We obtained approval from the Turgut Özal University Ethical Committee and followed the Helsinki Declaration principles. The UC patients were classified as ulcerative proctitis, left-sided (distal) UC, and extensive UC (pancolitis) according to the Montreal classification. ^[12] We used enhanced depth imaging (EDI) optic coherence tomography (OCT) at the foveal center and at 500 μm, 1000 μm, and 1500 μm from the foveal center temporally and nasally in each eye. All measurements were taken by the same ophthalmologist (AK) using the same OCT device (Heidelberg Engineering, Heidelberg, Germany). We took the measurements in the morning hours to eliminate the diurnal CT fluctuation. ^[13] We included patients followed up by the Gastroenterology Clinic with a diagnosis of UC who were in remission according to the Truelove and Witts Criteria. ^[14] The patients were on 5-aminosalicylic acid (ASA) (n = 22), azathioprine and 5-ASA (n = 12), and anti-transforming growth factor α (TNF α) (n = 2). A full ophthalmological examination including best-corrected visual acuity (BCVA) with the Snellen chart, intraocular pressure measurement with Goldmann applanation tonometry, biomicroscopy, and dilated fundus examination were performed in every participant. Only patients with a BCVA of at least 0.8 were included in the study.

Exclusion criteria were a spherical equivalent value >±2.0, a history of ocular surgery, ocular trauma, anterior or posterior segment disease, smoking and alcohol use, migraine, and a previous systemic or chronic disease such as hypertension and diabetes mellitus using any ocular drug and using any systemic drug other than azathioprine, 5-ASA, and anti-TNF α. These factors were considered to have an effect on the choroid and/or retina. ^[15]

Optic coherence tomography scan protocol

The method of obtaining EDI-OCT has been described previously. ^[16] We used a Heidelberg spectral-domain (SD) OCT (Heidelberg Engineering, Heidelberg, Germany) and software version 6.3.3.0. The SD-OCT contained a superluminescent diode with a wavelength of 870 nm. It was able to obtain 40.000 A-scans per second with an axial and transverse resolution of 7 and 14 μm, respectively. We used a 1 × 30° area at the fovea to obtain two horizontal line scans through the fovea at high quality. A total of 100 scans were averaged for each section. The automatic real-time averaging mode was used to maximize the signal-to-noise ratio and ensure high-quality images. We then evaluated the CT measurements using these images. We measured choroidal depth (the distance between the outer reflective retinal pigment epithelium layer and the inner sclera border) manually. We measured the sections horizontally across the fovea at 500 μm intervals. CT was measured horizontally at the subfoveal region with the digital calipers that the Heidelberg Spectralis software (Heidelberg Engineering, Heidelberg, Germany) provides. The points of measurement were 1.5 mm temporal and 1.5 mm nasal to the fovea.

Statistical analysis

Continuous variables were expressed as a mean ± standard deviation. The Kolmogorov-Smirnov test was used to verify normal distribution of the values before statistical analysis. The independent t-test was used for parametric statistical analysis. The Mann-Whitney U-test and Kruskal-Wallis variance analysis were used as nonparametric tests. The Chi-square test was used for group comparisons when indicated P < 0.05 was considered statistically significant.

Results

The ages and genders of the cases and controls were similar (P > 0.05) [Table 1].

Table 1: Demographic features of the ulcerative colitis patients and healthy control participants

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The CT was statistically significantly thinner in the UC patients than the controls at T500 (P = 0.026), N500 (P = 0.019), N1000 (P = 0.042), and N1500 (P = 0.013) [Table 2].

Table 2: Choroidal thickness values of the ulcerative colitis patients and healthy control participants

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There were 12 extensive, 17 left type, and 7 proctitis type UC patients in our study according to the Montreal classification. There was no statistically significant difference between these three groups regarding the CT value (P > 0.05) [Table 3].

Table 3: Ulcerative colitis types and choroidal thickness values according to the Montreal classification^[12]

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There were no correlations between CT (subfoveal choroidal thickness: P = 0.431, r = −0.142; T500: P = 0.195, r = −0.232; T1000: P = 0.406, r = −0.150; T1500: P = 0.697, r = −0.070; N500: P = 0.077, r = −0.312; N1000: P = 0.219, r = −0.220; N1500: P = 0.830, r = −0.039) and disease duration.

Discussion

The main characteristics of UC are increased levels of pro-inflammatory cytokines such as interleukin (IL)-1,-6,-8, and TNF α and decreased levels of the anti-inflammatory IL-10 with increased recruitment of leukocytes to the inflamed area. ^[3] It has been reported that the inflammatory response that is induced by a specific epithelial protein in the colon cross-reacts with antigens in the eyes, skin, joints, and biliary tract and therefore leads to the development of EIM. ^[17] Ocular complications include anterior uveitis, conjunctivitis, and episcleritis and usually occur in 2%-10% of UC patients. ^[5],[6],[18] They can also manifest before the intestinal problems and enable early diagnosis. One must therefore know the ocular signs well to prevent the significant problems they may cause. ^[19] These ocular UC complications are usually seen together with other extraintestinal signs and especially arthritis and erythema nodosum. It is thought that the similarity of the synovial and uveal microvascular structure is probably involved in this association as enhanced antigen presentation, migration of leukocytes and cytokine activity have been shown at both sites. ^[7],[17]

Furthermore, the increase in several inflammatory mediators such as IL-1 and TNF α in UC disrupt the fibrinolytic system and decrease activation of the natural anticoagulant pathway, leading to a hypercoagulable state and thrombus formation. ^[20] Thromboembolism usually develops in the venous circulation but sometimes also in the arterial circulation. Deep vein thrombosis and pulmonary embolism are the usual manifestations of thromboembolism but cerebral, retinal, and hepatic thromboses have also been reported. ^[21],[22]

The vascular endothelial dysfunction related to increased inflammation in UC patients has been shown to affect the retinal vascular structures and cause obstruction of the venous and arterial system. ^{[10],[11],[23],[24]} Other reports include retinal vasculitis and periphlebitis in UC patients. ^[9],[25] Bilateral retinal vasculitis with late phase venous leakage and retinal ischemia on fundus fluorescein angiography has been reported in a biopsy-proven active UC patient. ^[9] It is also possible for ocular complications to develop due to the effect of the vasculitis and pro-thrombotic changes on the eye's microvascular structure.

We found that perifoveal CT was statistically significantly thinner in UC patients in remission compared to the healthy control group. We believe that the reason is choroidal ischemia following thrombus development due to inflammation-related vascular endothelial dysfunction. Another possible cause is the ischemia developing with decreased choroidal blood flow as a result of narrowing of choroidal vascular structures due to the vasculitis. In addition, the lack of a difference in CT between the UC groups according to the Montreal classification could be because we measured the CT during remission.

Onal et al. ^[26] found no significant correlation between CT and clinical, laboratory, and endoscopic parameters of UC activity in contrast to our study. They reported that CT could not be used as a disease indicator for UC. However, they performed the CT measurements at three points as subfoveal and 3000 μm nasal and temporal to the fovea. We performed our measurements at seven points as subfoveal and at every 500 μm up to 1500 μm nasal and temporal to the fovea. It has been reported that choroidal vascularity can also be affected in patients suffering from rheumatoid arthritis (RA) where inflammatory mediators play a role in the pathophysiology and that retinal vasculitis can develop similar to UC. ^[27] Duru et al. ^[27] found that subfoveal and perifoveal CT was thinner than in the healthy control group in RA patients. They interpreted this as the immunological mechanisms that are active in RA leading to vascular inflammation that could be the precursor of choroidal vascular damage. Güngör et al. ^[28] also reported that posterior ocular sarcoidosis patients had lower CT than normal participants even where there was no active ocular inflammation, and the disease was quiet but could not find a satisfactory explanation.

Conclusions

Perifoveal CT was significantly thinner in UC patients than in healthy controls. However, the UC group according to the Montreal classification did not have a significant effect on the CT values. The limitation of our study is that CT evaluations were only made in UC patients in remission. Further comparative studies on larger series including active UC patients are needed for clarification of the matter.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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