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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 19  |  Issue : 1  |  Page : 46-52

The pattern of intraocular pressure elevation in a specialized uveitis clinic


Department of Ophthalmology, Kasr Alainy Hospital, Cairo University, Cairo, Egypt

Date of Submission07-May-2017
Date of Acceptance22-Aug-2017
Date of Web Publication1-Feb-2018

Correspondence Address:
Maha M Youssef
8 ElSamman Street, ElHaram, Giza 12561
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/DJO.DJO_36_17

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  Abstract 

Aim
The aim of this study was to determine the pattern and risk factors associated with elevated intraocular pressure (IOP) in patients attending a specialized uveitis clinic during a 6-month duration.
Materials and methods
A cross-sectional observational study was carried out in a specialized uveitis clinic, in Kasr Al-Aini Hospital, Cairo University. Patients with acute or chronic uveitis were included in the study. Patients with transient postoperative uveitis, masquerade syndrome, or presenting with glaucoma before the onset of uveitis were excluded. A comprehensive history was taken and all patients were subjected to full ophthalmological examination. Patients were considered to have ocular hypertension if the IOP was 21 mmHg or more without evidence of glaucomatous optic neuropathy or visual field changes, while those with evidence of glaucomatous optic neuropathy or visual field changes were considered to have secondary glaucoma.
Results
Eighty-four patients with a mean age of 30.76±12.77 years were included. The IOP was elevated in 35 (44 eyes) patients. Among 44 eyes, seven (15.9%) eyes developed glaucoma and 37 (84.1%) eyes were having ocular hypertension. Elevated IOP was significantly associated with closure of the anterior chamber angle (P<0.001), activity of the disease (P<0.001), and route of steroid intake (P<0.001).
Conclusion
Closure of anterior chamber angle, activity of inflammation, and route of steroid intake are considered as risk factors for the development of elevated IOP in uveitic patients. At-risk eyes should be monitored more frequently to avoid development of secondary glaucoma which represents a challenge.

Keywords: glaucoma, gonioscopy, ocular hypertension, risk factors, uveitis


How to cite this article:
Shaaban AM, Youssef MM, Eltanamly RM, AbdelAziz MS, Kotb MS. The pattern of intraocular pressure elevation in a specialized uveitis clinic. Delta J Ophthalmol 2018;19:46-52

How to cite this URL:
Shaaban AM, Youssef MM, Eltanamly RM, AbdelAziz MS, Kotb MS. The pattern of intraocular pressure elevation in a specialized uveitis clinic. Delta J Ophthalmol [serial online] 2018 [cited 2018 Apr 19];19:46-52. Available from: http://www.djo.eg.net/text.asp?2018/19/1/46/224562


  Introduction Top


Elevated intraocular pressure (IOP) is a frequent complication in uveitic patients. These patients are at greater risk than the normal population because of the nature of their disease and its potential to disrupt IOP homeostasis [1].

Uveitic ocular hypertension (OHT) must be differentiated from uveitic glaucoma, which is defined as elevated IOP resulting in progressive neuroretinal rim loss and/or perimetric glaucomatous field defects [2].

The purpose of this study was to determine the pattern and risk factors associated with elevated IOP in patients attending a specialized uveitis clinic, in Kasr Al-Aini Hospital, Cairo University, during a 6-month duration.


  Patients and methods Top


This cross-sectional observational study was carried out on consecutive patients attending a specialized Uveitis Clinic, in Kasr Al-Aini Hospital, Cairo University, from 1 March 2016 till 31 August 2016.

The study was approved by the Ophthalmology Department Ethics Committee and followed the Declarations of Helsinki of 1975 that were revised in 2000. Informed consent was obtained from all patients.

Patients with acute (<3-month duration) or chronic uveitis (≥3-month duration) were included in the study. Patients with transient postoperative uveitis, masquerade syndrome, or presenting with glaucoma before the onset of uveitis were excluded.

For the purpose of this study, the patients were considered to have OHT if the IOP was 21 mmHg or more on two separate occasions without evidence of glaucomatous optic neuropathy or visual field changes, while those with IOP more than or equal to 21 mmHg with evidence of glaucomatous optic neuropathy or visual field changes were considered to have secondary glaucoma. The authors used the term elevated IOP to refer to both the OHT and secondary glaucoma. Patients with OHT were monitored more closely for signs of onset of glaucoma. Humphrey visual field 24-2 (Humphery Perimeter; Zeiss, California, USA) was used to assess the visual field in those patients every 6 months.

A thorough and comprehensive history was taken from each patient. At each clinic visit, all patients were subjected to full ophthalmological examination including: corrected visual acuity for far using Snellen’s chart, anterior segment examination with slit-lamp, IOP measurement using Goldmann applanation tonometry, and posterior segment examination with indirect ophthalmoscopy and slit-lamp biomicroscopy using +90 diopter lens.

The authors adopted the Standardization of Uveitis Nomenclature (SUN) working group-updated method of grading anterior chamber cells and flare as follows [3].

For anterior chamber cells, in a slit beam of 1×1 mm, the following grades were standardized: 0 (<1 cell), 0.5+ (1–5 cells), 1+ (6–15 cells), 2+ (16–25 cells), 3+ (26–50 cells), and 4+ (>50 cells). The presence of hypopyon was recorded separately.

The grading for anterior chamber flare was described as follows: 0 (none), 1+ (faint), 2+ (moderate; iris and lens details are clear), 3+ (marked; iris and lens details are hazy), and 4+ (intense, fibrin or plastic aqueous).

For short-term assessment of therapy:
  1. Inactive anterior uveitis was described as grade 0 cells.
  2. Improvement was described as a two-step decrement in the grade of inflammation or a decrease to grade 0.
  3. Worsening activity was a two-step increment in the grade of inflammation or an increase from grade 3+ to 4+.


The degree of vitiritis was based on vitreal inflammatory cells, which are graded from 0 to 4+ according to their density [4].

In addition, uveitis was classified by anatomic location, according to the SUN Working Group 1, into the following [3]:
  1. Anterior uveitis.
  2. Intermediate uveitis.
  3. Posterior uveitis.
  4. Panuveitis.


Gonioscopy was done to determine the presence of peripheral anterior synechiae ([Figure 1]) and the extent of angle closure. Any angle abnormalities such as neovascularization, pigmentation, and fine vessels crossing the angle were recorded. Grading of the angle was done using ‘Shaffer’s system’ [5].
Figure 1: Anterior chamber angle showing peripheral anterior synechiae in a patient with elevated intraocular pressure.

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All medications used for treatment of inflammation and rise of IOP were recorded with the route administration and dose used. In general, the treatment begins with control of intraocular inflammation, which itself may normalize the IOP. In patients, where the IOP was not normalized by anti-inflammatory agents, medical and/or surgical therapy was used to control the IOP.

Statistical analysis

Data were coded and entered using the statistical package statistical package for the social sciences, version 23 (SPSS; SPSS Inc., Chicago, Illinois, USA). Data were summarized using mean, SD, median, minimum, and maximum in quantitative data and using frequency (count) and relative frequency (percentage) for categorical data. Comparisons between quantitative variables were done using the nonparametric Mann–Whitney test [6]. For comparing categorical data, χ2-test was performed. Exact test was used instead when the expected frequency is less than 5 [7]. P values of less than 0.05 were considered statistically significant.


  Results Top


Eighty-four patients presented to a specialized Uveitis Clinic, in Kasr Al-Aini Hospital, Cairo University, from 1 March 2016 till 31 August 2016. The mean age of the patients was 30.76±12.77 years (range: 6–65 years) and there were 60 (71.40%) male and 24 (28.60%) female patients.

Among the 84 patients, there were 147 uveitic eyes with bilateral uveitis in 63 (75%) patients and unilateral uveitis in 21 (25%) patients.

The majority of patients were diagnosed as having Behçet’s disease; 50 (34%) eyes followed by anterior granulomatous uveitis (with anterior chamber nodule) in 27 (18.3%) eyes and Vogt–Koyanagi–Harada (VKH) in 24 (16.32%) eyes ([Table 1]).
Table 1: Clinical entities of uveitis (original)

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The mean IOP was 18.29±6.86 mmHg (range: 9–55 mmHg). The IOP was found high (≥21 mmHg) in 35 (44 eyes) patients. Among the 44 eyes with elevated IOP, seven eyes of five (15.9%) patients developed glaucoma, and the remaining 37 (84.1%) eyes were having OHT.

Eighteen out of 50 (36%) eyes and seven out of 24 (29.2%) eyes developed elevated IOP in Behçet’s disease and VKH disease, respectively. Despite the fact that the only eye presenting with Posner–Schlossman syndrome and two eyes out of three eyes presenting with juvenile idiopathic arthritis which developed elevated IOP, one cannot state that those entities had the highest frequency of elevated IOP due to the small number of patients.

The authors tried to study the association between prevalence of elevated IOP and different risk factors namely anatomical classification of uveitis, pattern of uveitis (granulomatous vs nongranulomatous), course of uveitis, activity of disease, steroid use, and anterior chamber angle (open vs closed) as shown in [Table 2].
Table 2: Relation between high intraocular pressure and different risk factors (original)

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Posterior uveitis was found in 15 eyes (10.2% of uveitic eyes); anterior uveitis was found in 46 eyes (31.29% of uveitic eyes) and panuveitis was found in 82 eyes (55.78% of uveitic eyes). It was found that there was a trend of high IOP with panuveitis, but it did not reach statistical significance (P=0.063, χ2). Among the 44 uveitic eyes with high IOP, there were 32 (72.7%) panuveitic eyes.

It was found that 51 eyes presented with granulomatous uveitis, among them there were 27 eyes with anterior granulomatous uveitis (with anterior chamber nodule). No statistically significant difference was found between granulomatous and nongranulomatous uveitis regarding the prevalence of high IOP (P=0.393, χ2).

Elevated IOP developed in 39 out of 133 (29.3%) eyes and five out of 14 (35.7%) eyes in chronic and acute uveitic patients, respectively. There was no statistically significant difference between acute and chronic uveitis as regards the prevalence of high IOP (P=0.760, χ2).

It was found that there was a statistically significant association between the activity of the disease and elevation of the IOP in uveitic patients (P<0.001, Mann–Whitney). Among the 147 uveitic eyes, there were 47 eyes with active inflammation, among them there were 40 eyes with elevated IOP. Moreover, IOP was found to be positively correlated with the grade of inflammation (Spearman’s correlation: r=0.723, P<0.001).

The prevalence of high IOP in patients who received steroids was 33.3% (39 out of 117 eyes). There was a trend of high IOP with steroid use but it did not reach statistical significance (P=0.075, χ2). Among the 117 eyes that received steroids, there were 25 (21.4%) eyes treated with topical steroids, 78 (66.66%) eyes treated with systemic steroids, and 14 (11.96%) eyes treated with periocular steroids. There was a statistically significant relationship between elevation of IOP and the route of administration of the steroids (P<0.001). Among those who were treated by periocular steroids, 12 out of 14 (85%) eyes developed high IOP ([Table 3]).
Table 3: Association between high intraocular pressure and route of steroid administration (original)

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It was found that among 44 uveitic eyes with high IOP there were 28 (63.6%) eyes with open angle of the anterior chamber and 16 (36.4%) eyes with closed angle. There was a statistically significant (P<0.001, χ2) association between angle closure of the anterior chamber and raised IOP in uveitic patients.

There were seven eyes out of 147 (4.7%) uveitic eyes diagnosed as glaucoma. Trabeculectomy with mitomycin was done in three eyes, but the IOP was controlled only after adding antiglaucoma drugs. Decision of surgery had been taken by glaucoma consultants due to failure of control of IOP despite use of four topical medications and addition of systemic carbonic anhydrase inhibitor. The remaining four eyes were managed medically with standard topical and/or oral treatment. There was no statistically significant association between secondary glaucoma and previously mentioned risk factors.


  Discussion Top


The authors have conducted this study to understand better the pattern and associated risk factors with elevated IOP in patients attending a specialized uveitis clinic, during a 6-month duration. They reported the prevalence of elevated IOP to be 29.9% (44 out of 147 eyes), of OHT to be 25.17%, and secondary glaucoma to be 4.76%. Variable prevalence of elevated IOP has been reported in other studies due to the difference in study population, parameters used for glaucoma diagnosis, study duration, inclusion, and exclusion criteria [1],[8],[9],[10],[11].

The criteria the authors have used for glaucoma definition is more or less in agreement with the First International SUN Workshop. They reached a consensus that the term glaucoma should not be considered synonymous with elevated IOP in a uveitic patient, but that it should be reserved for those conditions where there is either demonstrated glaucomatous disk damage or documented visual field defect. The term elevated IOP should be used for those situations where there is an IOP above a defined normal range or when there is an increase in IOP from the baseline during a longitudinal study [3].

The authors’ findings regarding the overall prevalence of raised IOP approach the recent results from both Kanda et al. [8] and Mahajan et al. [9] in 2014, who reported the prevalence of OHT to be 25.4 and 21%, respectively. However, different prevalence has been reported in older studies. Herbert et al. [1] in 2004 found a higher prevalence of raised IOP in uveitic eyes (41.8%) and they found that raised IOP requiring treatment was 29.8% (102 out of 342 eyes). There were 33 (9.6%) eyes with a diagnosis of glaucoma. This difference could be attributed to different criteria used for the diagnosis of elevated IOP and different clinical entities of uveitis encountered in their study population [1]. On the contrary, Panek and colleagues in 1990 and Takahashi and colleagues in 2002 reported a lower prevalence of elevated IOP (19.3 and 18.3% of eyes, respectively). This difference may be attributed again to the difference in uveitis entities. Being a tertiary center, it was possible that the incidence of raised IOP among patients with acute uveitis was underestimated. A transient rise in pressure associated with the onset of inflammation that resolved with the initiation of treatment by the referring doctor may have been missed. In addition, they used the term glaucoma as synonymous with elevated IOP; however, this should have led to overestimation of glaucoma prevalence [10],[11]. Moreover, the study conducted by Takahashi et al. [11] is very different from the current one due to the long study duration (21 years) and huge sample size (1099 patients).

According to the clinical entity, the authors found that eighteen out of 50 eyes in Behçet’s disease, seven out of 24 eyes in VKH, and two out of eight eyes in Herpes virus-associated iridocyclitis developed elevated IOP. Merayo-Lloves et al. [12] showed that herpes virus-associated uveitis was most likely to cause secondary glaucoma followed by Fuchs’ heterochromic iridocyclitis, VKH, juvenile idiopathic arthritis, and sarcoidosis (12%). Takahashi et al. [11] had found that the prevalence of high IOP was 100% in Posner–Schlossman syndrome, 30.4% in Herpes virus-associated iridocyclitis, 20.8% in Behçet’s disease, 16.4% in VKH, and 15.1% in idiopathic uveitis. Elgin et al. [13] in 2004 had reported that the prevalence of secondary glaucoma in Behçet’s disease to be 10.9%. Kanda et al. [8] had found that the prevalence of high IOP was 100% in Posner–Schlossman syndrome, 50.0% in varicella zoster virus-associated iridocyclitis, 45% in scleritis, 34.1% in VKH, 32.1% in Behçet’s disease, 23.1% in acute anterior uveitis, and 20.2% in sarcoidosis.

The prevalence of high IOP in uveitic patients seems to be related to several factors including anatomical classification of uveitis, pattern and course of uveitis, activity of disease, steroid use, and anterior chamber angle.

Regarding the anatomical classification, IOP elevation was detected in 13.3% of eyes with posterior uveitis, in 21.7% of anterior uveitis, and in 37.2% of panuveitis. The prevalence of IOP elevation in posterior uveitis was lower probably due to the aqueous outflow pathway being less influenced by inflammation predominantly affecting the posterior segment [14]. It was found that panuveitis was the most common type that was associated with elevated IOP (72.72% of uveitic eyes with elevated IOP); however, this association did not reach statistical significance. This may be attributed to the presence of various factors that may predispose to high IOP including abnormality in anterior chamber angles in addition to these patients usually requiring different routes of steroid delivery including topical, periocular, and systemic. Different studies had investigated the relationship between the anatomical classification of uveitis and IOP elevation and did not find any significant relation [1],[15],[16], yet one study has shown that anterior uveitis was the most common clinical type associated with raised IOP (52.4%) [9].

Granulomatous uveitis was said to be associated with greater incidence of formation of peripheral anterior synechiae and hence a greater risk of OHT [9]. No statistically significant association, between high IOP and the histopathological type of the uveitis, was found in the current study. This was similar to the results in the study that was conducted by Mahajan et al. [9]. On the contrary, Merayo-Lloves et al. [12] and Saouli et al. [17] in 1999 reported that increased IOP and secondary glaucoma were more frequently observed in granulomatous uveitis. This could be due to the large number of patients in their studies and longer duration of follow-up [12],[17].

It is worth noting that no statistically significant association was detected between the course of the disease and raised IOP, in the present study. On the contrary, Herbert et al. [1] reported higher prevalence of raised IOP in chronic uveitis when compared with acute uveitis. Mahajan et al. [9] in 2009 reported a higher mean duration of disease process in patients with secondary glaucoma compared with uveitic patients without glaucoma in their study. However, this finding did not reach statistical significance [9].

The association between the elevation of IOP and activity of inflammation was found to be statistically significant, in the present study. This conclusion is in agreement with other studies [1],[11],[17]. High IOP in the absence of active inflammation may be secondary to angle closure and that is why the angle of anterior chamber was evaluated in each patient.

The majority of the patients were having open angles on gonioscopy; however, there was a statistically significant association between closure of the anterior chamber angle and raised IOP. Gonioscopic findings have been evaluated by only few studies in the literature. Open angles have been reported in the majority of eyes [9],[11],[12].The diagnosis of steroid-induced glaucoma is made based on: (a) an IOP increase in parallel with the use of topical or systemic steroids and (b) a decrease in IOP with discontinuation of the steroids. The use of steroid at the onset of inflammation is generally agreed upon, with the possibility of coupling them with immunosuppressant therapy. Steroids should be tapered whenever possible, guided by clinical criteria to avoid serious side effects. It is postulated that steroid therapy of more than 6 months represents an additional risk to develop glaucoma [9].

In the current study, there was a trend of high IOP with steroid use but it did not reach statistical significance. Takahashi et al. [11] found that the proportion of steroid-induced glaucoma was 8.9% (26 out of the 293 eyes with secondary glaucoma),while Herbert et al. [1] reported that corticosteroid use was positively correlated with raised IOP. On the contrary, Panek et al. [10] did not report any case of raised IOP secondary to steroid response. Similarly, Saouli et al. [17] had noted corticosteroid-induced IOP rise in only two cases out of 45 cases of OHT.

In the present study, it was found that 85% of uveitic eyes treated by periocular steroids developed high IOP. Sijssens et al. [16] recorded elevated IOP in 35% of children with pediatric uveitis during a follow-up of 5 years. They found raised IOP to be significantly more frequent following periocular steroid injection although the number of injections did not bear any significance and systemic steroids were not found to be of any influence [16]. Mahajan et al. [9] reported the prevalence of steroid-related IOP rise to be 28.6% in 42 patients with uveitic glaucoma. They found a significant association between prevalence of raised IOP and topical, periocular, and systemic steroid use [9].

In summary, this study concluded that elevated IOP occurred in 29.93% (44 eyes of 147 uveitic eyes) in a specialized uveitis clinic, during a 6-month duration. Elevation of IOP was significantly associated with the closure of the anterior chamber angle, the activity of the disease, and the route of steroid intake. These risk factors for elevated IOP should enable closer monitoring of ‘at-risk’ eyes and early and proper management of these eyes that might develop a secondary uveitic glaucoma, which represents a challenge in its management. We do appreciate that this study had many limitations, the most important of which are the small sample size and short study period.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Herbert HM, Viswanathan A, Jackson H, Lightman SL. Risk factors for elevated intraocular pressure in uveitis. J Glaucoma 2004; 13:96–99.  Back to cited text no. 1
    
2.
Moorthy RS. ‘Complications of uveitis’ intraocular inflammation and uveitis. San Francisco; CA: American Academy of Ophthalmology; 2016. 291–300  Back to cited text no. 2
    
3.
Jabs DA, Nussenblatt RB, Rosenbaum JT, Standardization of Uveitis Nomenclature Working Group. Standardization of uveitis nomenclature for reporting clinical data: results of the first international workshop. Am J Ophthalmol 2005; 140:509–516.  Back to cited text no. 3
    
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Dunn JP. Uveitis. Prim Care 2015; 42:305–323.  Back to cited text no. 4
    
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Kanda T, Shibata M, Taguchi M, Ishikawa S, Harimoto K, Takeuchi M. Prevalence and aetiology of ocular hypertension in acute and chronic uveitis. Br J Ophthalmol 2014; 98:932–936.  Back to cited text no. 8
    
9.
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Takahashi T, Ohtani S, Miyata K, Miyata N, Shirato S, Mochizuki M. A clinical evaluation of uveitis-associated secondary glaucoma. Jpn J Ophthalmol 2002; 46:556–562.  Back to cited text no. 11
    
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Merayo-Lloves J, Power WJ, Rodriguez A, Pedroza-Seres M, Foster CS. Secondary glaucoma in patients with uveitis. Ophthalmologica 1999; 213:300–304.  Back to cited text no. 12
    
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Elgin U, Berker N, Batman A. Incidence of secondary glaucoma in Behçet disease. J Glaucoma 2004; 13:441–444.  Back to cited text no. 13
    
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Kok H, Barton K. Uveitic glaucoma. Ophthalmol Clin North Am 2002; 15:375–387.  Back to cited text no. 14
    
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Neri P, Azuara-Blanco A, Forrester JV. Incidence of glaucoma in patients with uveitis. J Glaucoma 2004; 13:461–465.  Back to cited text no. 15
    
16.
Sijssens KM, Rothova A, Berendschot TT, de Boer JH. Ocular hypertension and secondary glaucoma in children with uveitis. Ophthalmology 2006; 113:853–859.  Back to cited text no. 16
    
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Saouli N, Brézin AP. Ocular hypertension and uveitis. Study of 374 cases of uveitis. J Fr Ophthalmol 1999; 22:943–949.  Back to cited text no. 17
    


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