|Year : 2012 | Volume
| Issue : 3 | Page : 314-319
Effects of inhaled fluticasone on intraocular pressure and central corneal thickness in asthmatic children without a family history of glaucoma
Muslim M Alsaadi1, Uchechukwu L Osuagwu2, Turki M Almubrad2
1 Department of Pediatrics, College of Medicine, King Khalid University Hospital, King Saud University, Saudi Arabia
2 Department of Optometry and Vision Sciences, Corneal Research Chair, College of Applied Medical Sciences, King Saud University, Saudi Arabia
|Date of Web Publication||3-Jul-2012|
Uchechukwu L Osuagwu
Cornea Research Chair, Department of Optometry and Vision Sciences, College of Applied Medical Sciences, King Saud University, PO Box-10219, Riyadh-11433
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Purpose: The aim of this study is to report the effects of fluticasone-inhaled corticosteroid on intraocular pressure (IOP) and central corneal thickness (CCT) of asthmatic children without a family history of glaucoma.
Materials and Methods: In this prospective study, 93 children were divided into two groups: 69 asthmatic children with no family history of glaucoma who were taking inhaled fluticasone propionate 250 μg daily for at least 6 months (Group 1) and 24 age-matched control subjects without asthma (Group 2). Three measurements each, of IOP and CCT, were performed with a hand-held noncontact tonometer and a noncontact specular microscope, respectively, over a 12-week period. The order of IOP and CCT measured were randomized at each visit. Between-group comparison and the relationship between CCT and IOP measurements were investigated. P < 0.05 was statistically significant.
Results: The mean age was 8 ± 2.4 years (range, 5−15 years) and 9 ± 2.9 years (range, 5−15 years) for Groups 1 and 2, respectively (P = 0.1337). The mean IOP was 14 ± 3.3 mmHg (range, 10−24 mmHg) and 14 ± 2.9 mmHg (range, 11−22 mmHg) for Groups 1 and 2, respectively (P = 0.3626). The mean CCT was 531 ± 30.1 μm (range, 467−601 μm) and 519 ± 47.0 μm (range, 415589 μm) for Groups 1 and 2, respectively (P = 0.1625). There was a weak but statistically significant correlation between IOP and CCT in Group 1 (Pearson's R = 0.3580, P = 0.0025).
Conclusions: Inhaled fluticasone at the regular dose used in this study over a short period (6-24 months) was not associated with a significant effect on CCT and IOP measured with noncontact devices in asthmatic children between 5 and 15 years, without a family history of glaucoma. A weak correlation between IOP and CCT values in asthmatic children did exist.
Keywords: Asthma, Corneal Thickness, Fluticasone Propionate, Inhaled Corticosteroids, Intraocular Pressure
|How to cite this article:|
Alsaadi MM, Osuagwu UL, Almubrad TM. Effects of inhaled fluticasone on intraocular pressure and central corneal thickness in asthmatic children without a family history of glaucoma. Middle East Afr J Ophthalmol 2012;19:314-9
|How to cite this URL:|
Alsaadi MM, Osuagwu UL, Almubrad TM. Effects of inhaled fluticasone on intraocular pressure and central corneal thickness in asthmatic children without a family history of glaucoma. Middle East Afr J Ophthalmol [serial online] 2012 [cited 2019 Aug 19];19:314-9. Available from: http://www.meajo.org/text.asp?2012/19/3/314/97936
| Introduction|| |
Asthma is a complex syndrome characterized by airway hyper-responsiveness (AH) caused by a multi-cellular inflammatory reaction that leads to airway obstruction. , The prevalence of asthma in Saudi Arabia has been increasing,  and was reported to have affected 2 million individuals of Saudi Arabian origin in 2001.  This high prevalence of asthma in Saudi Arabia coupled with several other factors such as the poor general knowledge of primary care physicians on asthma control, reluctance to prescribe control medications, led to the publication of the Saudi Initiative for Asthma (SINA). 
Inhaled corticosteroids (ICS) are currently the most effective anti-inflammatory medications commonly used in the treatment and management of mild to moderate asthma. A direct relationship between topical, systemic corticosteroids, and elevated intraocular pressure (IOP) has been recognized for more than five decades. , The extent to which these corticosteroids influence the IOP remains controversial. Generally, it is well known that steroids can cause an elevation of IOP, whether they are administered topically or systemically over a long period of time. ,,
A thin central cornea and increased IOP have been identified as major risks factor in the development of glaucoma and ocular hypertension. ,,, Evaluation of central corneal thickness (CCT) is important as it can be a sensitive indicator for a wide range of disorders which affect the anterior segment and the cornea, including glaucoma. ,
The introduction of noncontact measurement of IOP and CCT has resulted in widespread attention to these parameters in many optometry clinics. However, contact devices (Goldmann applanation tonometer, GAT, and ultrasound pachymeter, USP) are still the preferred method for measurement of IOP and CCT. , USP and GAT are still regarded as the gold standard of care, even though local anesthesia is required and measurement in children is challenging. However, the advantage of noncontact devices is increased convenience of measuring IOP and CCT without touching the anterior surface. This therefore negates the need for topical anesthesia and eliminates the risk of cross-contamination that can transmit ocular infections. The noncontact methods enable easier and faster screening of IOP and CCT in optometry clinics.
The majority of information on the pathogenesis of asthma is based on studies performed in young adults. Due to numerous complications, studies in infants and the pediatric age group are often difficult to conduct; therefore, there is relative paucity of information in this age group. We assessed the IOP and CCT of a cohort of asthmatic children, who were managed primarily with ICS therapy. The aim of this study was to reliably determine any eye adverse effects on IOP and CCT from the use of ICS to control asthma in a population of young children without a family history of glaucoma. The outcomes of this study may assist in early and intensive monitoring of asthmatic patients to prevent anatomic ocular damage and help prevent visual impairment.
| Materials and Methods|| |
A 12-week prospective, observational study was conducted at the pediatric pulmonology clinic of Dallah Hospital, Riyadh, Saudi Arabia. Subjects gave informed consent to participate in this study. This study was conducted according to the tenets of declaration of Helsinki and was approved by the institutional research ethics review board of the College of Applied Medical Sciences, and the management board of Dallah Hospital.
The study cohort comprised 93 subjects who were divided into two groups: Group 1 included 69 asthmatic children (37 (54%) males and 32 (46%) females) aged 8 ± 2.4 years (range, 5−15 years) with no family history of glaucoma; Group 2 included 24 age-matched control subjects [14 (58%) boys and 10 (42%) girls] aged 9 ± 2.9 years (range: 5−15 years). Participants in this study comprised patients from the out-patient pulmonary clinic of Dallah Hospital either for the management of asthma or their accompanying relatives who were confirmed healthy by the pediatric pulmonologist. Data from Group 2 (the control group) was used to validate the findings and changes in the Group of asthmatic children (Group 1).
Inclusion criteria for Group 1 were, age 5 years or older, compliant (as indicated by their regular follow-up visits) on only fluticasone propionate (Flexotide, Glaxo SmithKline, UK) 250 μg daily for more than 6 months. In all participants, fluticasone propionate was administered with the aid of an aero-chamber to ensure that the therapeutic dose required was delivered to the lungs. Inclusion criteria for Group 2 were age 5 years and healthy without any history of pulmonary disease. Prior to inclusion in the study, each subject underwent a comprehensive ophthalmic examination which included slit-lamp biomicroscopy of the external eye and anterior segment, direct ophthalmoscopy, automated refraction and pupil evaluation. Subjects with a positive history of one of the following were excluded: a positive history of (or objective evidence of) anterior segment disease or surgery, a history of contact lens wear, a history or positive family history of glaucoma, and evidence of cataract. Patients were also excluded if they experienced any deterioration that resulted in hospitalization or treatment with additional ICS, or if they used topical nasal steroid or other steroids for any other indication during this study.
Intraocular pressure and corneal thickness measurements
IOP was measured with the PT100 NCT (Reichert Technologies, Depew, New York, USA) and CCT measurement was performed with the SP-3000P noncontact specular microscope (Topcon Corp., Tokyo, Japan). Other methods of IOP measurement such as Goldmann applanation tonometry are difficult and often impossible to perform on young children because of the contact of the probe with the eye and lack of cooperation − hence the choice of instruments in this study.
The IOP was measured in the right eye of each subject by one clinician (TA) and another clinician (UO) performed measurements of CCT on the same eye. To determine which variable was measured first, the procedure of measurement was randomized resulting in some subjects undergoing CCT measurements before IOP measurements and vice versa. This was adopted to avoid tactile clues which might aid the tonometrist to determine the endpoint of a reading.
Three repeat IOP measurements were performed with the PT100 and averaged. Only good quality measurements as described by the manufacturer - "a good bell-shaped pressure signal with tall, relatively equal applanation peaks and relatively smooth raw and filtered applanation signals" − were recorded and averaged in each subject for statistical analysis. For some subjects, up to seven measurements were performed in order to obtain three good quality readings. The procedure adopted for measurement of IOP was as recommended by the manufacturer, to conform to the principle of IOP measurement of the Reichert PT100 noncontact tonometer. With this noncontact tonometer, a pulse of air is first delivered to the cornea and subsequent pulses are automatically adjusted to the IOP of the cornea to minimize the risk of excessive air pressure.
Three repeat measurements of CCT were obtained using the automatic mode of the Topcon SP-3000P noncontact specular microscope after the subject has been properly aligned (chin rested on the chin rest, head on the forehead rest, and patient looking straight ahead).
Due to the influence of diurnal variation in IOP , and CCT,  all measurements were made between 12:00 hours and 14:00 hours Riyadh time for all subjects.
The average IOP and CCT of each subject formed the data points used for the statistical analyses.
The levels of IOP and values of CCT for the two groups were the continuous variables. Both variables were analyzed using descriptive statistics (mean and standard deviation). Student's t-test or Mann−Whitney test was used where appropriate to compare means from the two independent groups. The relationship between CCT and IOP was investigated using the Pearson's correlation coefficient. The level of statistical significance was set at 5%. All statistical analyses were conducted using the Graph-pad Instat Version 3 for Windows (Graph pad Software Inc., San Diego, CA, USA). To achieve a statistical power of 80% at an α level of 0.05, 77 subjects were required. This sample size calculation was determined from an initial sample of 15 subjects using the statistical freeware G*Power (version 3.0.5).
| Results|| |
The study included 69 asthmatic children (Group 1) and 24 aged-matched controls (Group 2). The mean age for Group 1 was 8 ± 2.4 years (mean ± SD) and for Group 2 9 ± 2.9 years. There was no statistically significant difference in the mean age between groups (unpaired t-test, P = 0.1337).
In Group 1, the mean IOP was 14 ± 3.3 mmHg (range, 10−24 mmHg) and 14 ± 2.9 mmHg (range, 11−22 mmHg) for Group 2. Within Groups 1 and 2, IOP varied by an average of 0.1 ± 1.0 mmHg (95% confidence interval, CI: −2.0 to 2.0 mmHg) and −0.1 ± 0.8 mmHg (95% CI: −1.5 to 1.7 mmHg), respectively. There was no statistically significant difference in IOP measurements between groups (Mann−Whitney U test: P = 0.3626). The median IOP was 13 mmHg in both groups.
Of the Group 1 subjects, 66 (96%) children had IOP measurements within the normal range (10 and 21 mmHg), and 3 subjects had IOP above 21 mmHg. In these subjects, two (3%) had IOP of 23 mmHg, and one (1%) had IOP of 24 mmHg. Further examination at the King Saud University ophthalmology clinic, Saudi Arabia, revealed no other associated glaucoma changes. In Group 2, one child (4%) had an IOP of 21 mmHg; the remainder of the subjects had an IOP ranging from 11 to 20 mmHg.
The mean corneal thickness in Groups 1 and 2 was 531 ± 30.1 μm (range, 467−601 μm) and 519 ± 47.0 μm (range, 415−589 μm), respectively. Within-subject variability in corneal thickness ranged between −14 and 14 μm in Group 1 and −10 and 12 μm in Group 2. There was no statistically significant difference between groups (unpaired t-test, P = 0.1625).
[Figure 1] shows a scatter graph of association between CCT and IOP in the treatment group. There was a weak but statistically significant association between IOP and CCT in Group 1 (Pearson's r = 0.3580, P = 0.0025). [Figure 2] presents the scattergram of IOP and CCT in normal children.
|Figure 1: The relationship between IOP and CCT of 69 asthmatic children with no family history of glaucoma, compliant on a 250 μg daily dose of fluticasone propionate for ≥ 6 months (Pearson's r = 0.3580, P < 0.01)|
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|Figure 2: Correlation between the level of IOP and CCT of 24 normal children (Pearson's r = 0.2998, P > 0.05)|
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| Discussion|| |
Ocular hypertension has been recognized as the most important risk factor for the development of primary open-angle glaucoma. ,,, The standard definition or ocular hypertension is increased IOP greater than two standard deviations above 21 mmHg (mean = 16 mmHg, normal range 10−21 mmHg) in the absence of optic nerve damage or visual field loss.  Similarly, a thin central cornea has also been demonstrated as a strong predictive factor in the development of primary open angle glaucoma in the ocular hypertensive treatment study.  In the ocular hypertensive treatment study, subjects with primary open-angle glaucoma showed slightly lower CCT than normal subjects.
Evaluating the effect of ICS on IOP and CCT is therefore necessary to ensure that asthmatic children who are managed with continuous ICS are not at risk of developing ocular hypertension or glaucoma. A review of the recent literature has shown that over 80% of patients prescribed topical glucocorticoids are fearful of side effects ("steroid phobia") and fail to use them appropriately. This lack of compliance leads to decreased therapeutic benefits. 
Studies concerning glaucoma or elevated IOP with ICS in asthmatic children are limited and have yielded controversial results. In a recent study,  the intermittent use of intranasal budesonide in the treatment of allergic rhinitis, at an average daily dose of 100 μg over a period of 2 years, was not associated with ocular side effects such as cataract, glaucoma, corneal ectasia, and abnormal tear function in 150 children aged between 8 and 15 years. To validate their findings, the investigators  enrolled a control group of 90 patients who were newly diagnosed as having allergic rhinitis without any treatment. Similarly, in the current study, corticosteroid administered as inhaled fluticasone propionate at a treatment dose of 250 μg daily in children between the ages of 5 and 15 years, with no family history of glaucoma, was well tolerated and safe. For example, the median IOP of the study group (13 mmHg; range, 10−24 mmHg) did not vary significantly from the control group (13 mmHg, range, 11−22 mmHg). Of note also is the fact that 7 out of the 69 patients enrolled in this study had been on a regular daily dose of 250 μg of fluticasone ICS for 6 years or longer. In these 7 patients, IOP and CCT measurements were <15 mmHg and <500 μm, respectively. The findings of the current study concur with the literature that has reported no significant effect in the IOP of pediatric asthmatic patients that were being managed over the long term ,,,,, or short term  using normal therapeutic dosage of ICS. Garbe et al.  in an investigative study of 40,000 patients found no association with the use of ICS and open-angle glaucoma or increased risk of ocular hypertension. A similar finding was reported in a prospective study of 187 patients on ICS therapy that had various pulmonary conditions but with no history of glaucoma. The results indicated no significant increase in IOP in these patients.
In contrast, studies linking the association of ICS to increased IOP in children are limited to a handful of isolated case reports.  In one study  on patients aged ≥ 66 years prescribed high doses of ICS for >3 months, an increased risk of ocular hypertension or open angle glaucoma was reported. Mitchel et al.  in their letter to the editor concluded that all users of steroids are high IOP risk subjects, particularly those with positive family histories. In their 2 year cross-sectional, population-based study of 3654 persons between 49 and 97 years of age, an increase in IOP was observed in 328 subjects between 21and 75 years of age who used inhaled or intranasal steroids and had positive family histories of glaucoma or elevated IOP. In our study, patients with no family history of glaucoma who were on a therapeutic daily dose of 250 μg of fluticasone propionate for ≥6 months showed no increase in IOP in comparison to healthy non-asthmatic patients. We therefore tend to disagree with the generalization that "all steroid users are at high risk of developing open angle glaucoma." While this statement might be true for patients with a positive family history of glaucoma and other risk factors for IOP elevation after steroid treatment,  however our study and various other studies ,,,,, have shown that the use of ICS is safe at a therapeutic dosage in patients with no family history of glaucoma.
However, caution should be taken in the interpretation of our findings. In the present study, asthmatic children on a maintenance dose (250 μg) of fluticasone were only monitored for a short period of time. Their exposure period could not be accurately ascertained in all patients. High-to-medium-dose ICS have been associated with an increase in IOP  and development of cataract  in the past. In one of the studies  on 116 asthmatic children of ages 5−10 years placed on different doses of budesonide, IOP increased in 3 of the children from the baseline IOP value of 18−19 mmHg to 23 mmHg, 25 mmHg, and >28 mmHg, respectively. This therefore could suggest that there could be an increase in efficacy; children should be carefully monitored for ocular adverse effects in the cases where it becomes necessary to increase the dose of ICS above the normal therapeutic doses.
We found that the mean CCT did not vary (P > 0.05, unpaired t-test) between the two groups. The mean CCT obtained in both groups (519 ± 47.0 μm, 531 ± 30.1 μm; Groups 1 and 2, respectively) was comparable to that found in other studies on children , considering that the noncontact specular microscope which was used in this study underestimates CCT values in comparison to ultrasound pachymetry. 
Though this study was not designed to evaluate the association of cataract with the use of inhaled fluticasone, no eyes in the cohort developed any lens opacities on ophthalmological evaluation within the study period. This could be due to the fact that the subjects were not followed for a longer period. Nevertheless, 7 (10%) of the subjects enrolled in Group 1 had been using ICS for ≥ 6 years and showed no evidence of cataract on ophthalmological evaluation, further confirming the report of previous studies ,,, which have demonstrated the lack of association of ICS with posterior sub-capsular cataract.
IOP in healthy children is lower than that in adults. At age 12, the IOP is the same as that in an adult (average 12 mmHg).  The mean IOP observed in our study is similar to that reported by other studies that evaluated a pediatric study cohort. ,, Three (4%) children in our study group had an unexplained IOP reading above 20 mmHg and mean CCT values of 512, 571, and 542 μm, respectively, which did not vary on the second measurement session after 1 week. No optic disc changes were noticed in these patients on ophthalmological evaluation.
The lack of ocular side effects in our study could be explained partly by the lower bioavailability and extensive metabolism of fluticasone propionate, as has also been reported in a previous study. 
Considering the high prevalence of asthma in Saudi Arabia, ,, the results of this study may be limited by the small sample size. A study on a larger population of children is needed in order to verify the findings of this study. To draw inferences on the effect of family history, it might also be useful to compare a group with a positive family history with a group with a negative family history. Our study period was conducted over a relatively short duration and there may be side effects of ICS but the usage duration was too short to reveal adverse events. Further prospective studies to evaluate the ocular effect of ICS when used for a longer duration by children with asthma might also aid in the understanding of the safety of these lifetime medications. Due to the uncooperative nature of children and poor fixation during measurement of IOP by GAT, the noncontact tonometer was used in this study. Hence, another setback to the findings of the current study is that historically, noncontact tonometers are not considered to be an accurate method of measuring IOP but instead a fast and simple way to screen for high IOP.  CCT has a greater effect on IOP measurements obtained by noncontact tonometers than GAT, , with a greater probability of overestimating IOP in thick corneas and underestimating IOP in thin corneas. However, noncontact tonometers are more accurate in pressure range less than 20 mmHg. 
With the reports of the increasing prevalence of asthma and the need for its long-term management using corticosteroids or other anti-inflammatory and anti-histaminic agents, it is important for healthcare practitioners to evaluate the variation in the IOP of these patients, if any, from normal subjects during treatment. This will help to ease the continuous fear of possible ocular side effects commonly expressed by guardians/parents of these children. It might also assist in the early and intensive monitoring of asthmatic patients to prevent anatomic ocular damage if the risk exists and thereby aid in the prevention of any visual impairment.
In conclusion, the result of this study shows that despite "steroid phobia," proper use of inhaled fluticasone in its regular therapeutic dose over a short period of time (6-24 months) has no significant effect on IOP and CCT obtained by noncontact devices in asthmatic children between the ages of 5 and 15 years, who have no family history of glaucoma. Also, there was a weak but statistically significant relationship between the level of IOP and central cornea thickness in the asthmatic children used in this study.
| Acknowledgments|| |
We acknowledge the management of Dallah Hospital Riyadh, Saudi Arabia, for their support during data collection.
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[Figure 1], [Figure 2]