European Archives of Oto-Rhino-Laryngology https://doi.org/10.1007/s00405-017-4846-7
RHINOLOGY
Evaluation of choroidal thickness in children with adenoid hypertrophy Taliye Cakabay1 · Selin Üstün Bezgin1 · Sadık Etka Bayramoglu2 · Nihat Sayin2 · Murat Kocyigit1 Received: 13 November 2017 / Accepted: 8 December 2017 © Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract Objective To assess choroidal thickness in children with adenoid hypertrophy versus normal controls using enhanced depth imaging optical coherence tomography (EDI-OCT). Methods Twenty-six children (left and right eyes, total 52 eyes), which were scheduled to adenoidectomy with severe adenoid hypertrophy and 26 age, sex and body mass index-matched healthy subjects (left and right eyes, total 52 eyes) were included in the study. Choroidal thicknesses (CT) were evaluated using enhanced depth imaging optical coherence tomography. The CT measurement was taken at the fovea and 1000 μ away from the fovea in the nasal and temporal regions. The macular retinal thickness was also measured. Results There was no statistically significant difference in the CT of all regions between the groups (p > 0.05). No statistically significant difference was found between two groups in terms of macular choroidal thickness (p > 0.05). Conclusion These results revealed that severe adenoid hypertrophy did not cause a significant effect on choroidal thickness. Short-term exposure to obstructive symptoms in children and preserved sympathetic–parasympathetic balance may explain this result. Keywords Adenoid hypertrophy · Choroidal thickness · Sleep-related disorder breathing · Obstructive sleep apnea
Introduction The vascular support of the outer part of the retina is provided by the choroid [1]. The smooth muscles of the choroid vessel walls are innervated by sympathetic and parasympathetic nerves. Choroidal blood flow has been shown to have a capacity to autoregulation [2]. It has been mentioned that choroidal thickness (CT) may be an indirect biomarker for choroidal circulation [3]. A structural and functional normal choroid is essential for retinal health [2]. Enhanced depth imaging optical coherence tomography (EDI-OCT) is a relatively new technique. It uses light with a longer wavelength for choroidal scanning and gives valuable data about choroidal morphology [4].
* Taliye Cakabay
[email protected] 1
Otolaryngology Clinic, Kanuni Sultan Suleyman Training and Research Hospital, Istanbul, Turkey
Ophthalmology Clinic, Kanuni Sultan Suleyman Training and Research Hospital, Istanbul, Turkey
2
Adenoid hypertrophy is one of the most common cause of pediatric upper airway obstruction and leads to sleep-related breathing disorder (SRBD) condition that ranges from upper airway resistance syndrome (UARS) to obstructive sleep apnea syndrome (OSAS). Patients with UARS have complaints such as snoring, mouth breathing, sleep pauses or breath holding, gasping, restless sleep, enuresis. Polysomnography is a gold standard test for evaluation of the severity and presence of obstructive symptoms. However, it is expensive, time-consuming and difficult to apply to children. Thus, usually the diagnosis of pediatric OSAS can be made based on physical findings, parenteral reports of nocturnal symptoms and nocturnal video recordings [5]. Many studies have studied choroidal thickness measurements in adults with OSAS [2, 6–11] and the metanalysis, which evaluated these studies revealed the significant reduction of choroidal thickness in OSAS [3]. It was suggested that intermittent airway obstructions in OSAS cause recurrent hypoxia and reperfusion episodes, which can lead to activate the sympathetic system, vascular dysregulation, abnormal choroidal flow and decreased choroidal thickness [3]. However to the best of our knowledge, there is no
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study to assess choroidal thickness in pediatric upper airway obstruction and/or OSAS. The aim of this study is to assess choroidal thickness in children with adenoid hypertrophy versus normal controls using enhanced depth imaging optical coherence tomography (EDI-OCT).
Materials and methods The study was approved by the Clinical Research Ethics Committee (Approval No. 2016.2.9). A written informed consent was obtained from the participants. The study was conducted in accordance with the principles of the Declaration of Helsinki. Children between the ages of 6–16 with obstructive complaints such as snoring, chronic nasal obstruction, oral respiration and pausing of breathe during sleep were included in the study. All subjects were evaluated by anterior rhinoscopy and flexible endoscopy. Adenoid hypertrophy levels were graded into four classes according to Cassano et al. criteria [12]. Adenoid hypertrophy causing airway obstruction classified into Grade-1 25%, Grade-2 25–50%, Grade-3 50–75% and Grade-4 75–100%. Patients, scheduled to adenoidectomy with grade 3 and 4 adenoid hypertrophy (severe adenoid hypertrophy) were included in the study. Parental reports of nocturnal symptoms were asked and nocturnal video recordings were evaluated. Choroidal thicknesses of 26 children (left and right eyes, total 52 eyes) with severe adenoid hypertrophy and 26 age, sex and body mass index-matched healthy subjects (left and right eyes, total 52 eyes) were measured by optical coherence tomography after detailed ophthalmologic examination. We excluded patients with nasal septal deviation, tonsillary hypertrophy (Grade 3–4, according to Brodsky scale [13]), history of previous adenoidectomy, chronic disease, regular drug use, head and neck malformations, allergic symptoms, passive smokers, high myopia or hyperopia (> + 3 or − 3 diopters of spherical equivalent), a history of intraocular surgery, ocular trauma, uveitis, any topical medication and poor image due to unstable fixation.
Ophthalmologic examination All participants underwent a detailed ophthalmic examination including slit-lamp biomicroscopy, tonometry, and fundus examination. All participants also underwent central corneal thickness (CCT) and axial length (AL) measurements using an ultrasonic scan. All examinations were performed between 9 a.m. and 12 a.m. All participants were examined by the Cirrus HD-OCT 4000 (Carl Zeiss Meditec, Inc., Dublin, CA).The CT measurement was taken at the fovea and 1000 μ away from the fovea in the nasal (N1) and temporal (T1) regions. The
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images were taken and assessed by two experienced ophthalmologist (NS and SEB). Both of them were masked in terms of groups. The macular retinal thickness (central 1000 μ thickness of fovea) was also measured using the Cirrus HD-OCT 4000 (Carl Zeiss Meditec, Inc., Dublin, CA).
Statistical analysis Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS) version 18 software (SPSS Inc., Chicago, IL, USA). Descriptive data were expressed in mean ± standard deviation. The normality of the data was confirmed by the Kolmogorov–Smirnov Z test. An independent t test and Mann–Whitney U test were used to compare variables among groups. A p value of 0.05) (Table 1). The mean subfoveal, nasal, and temporal CT values in adenoid hypertrophy group were 291.06 ± 50.21, 265.28 ± 57.76, 290.04 ± 57.91, respectively, and 282.89 ± 50.69, 257.17 ± 51.95, 281.10 ± 56.98 in the control group, respectively. There was no statistically significant difference in the CT of all three regions between the groups (p > 0.05) (Table 2). The medium macular thickness in the fovea was 241.38 ± 23.87 in the adenoid hypertrophy group and 232.88 ± 20.37 in the control group. No statistically Table 1 Demographic and ophthalmological characteristics of the groups Adenoid hypertrophy Control Eye (n) Age (years)
52 8.88 ± 2.24 (range 7–16) Male/female 28/24 BMI (kg/m2) 18.81 ± 6.05 SE 0.15 ± 0.61 AL (mm) 22.73 ± 0.1.03
52 9.07 ± 1.67 (range 6–13) 22/30 20.16 ± 6.49 0.3 ± 1.39 22.98 ± 0.93
p value 0.622 0.696 0.402 0.590 0.238
BMI body mass index, SE spherical equivalent, AL axial length
European Archives of Oto-Rhino-Laryngology Table 2 Choroidal thickness at different positions
Subfoveal Nasal Temporal
Adenoid hypertrophy
Control
p value
291.06 ± 50.21 265.28 ± 57.76 290.04 ± 57.91
282.89 ± 50.69 257.17 ± 51.95 281.10 ± 56.98
0.430 0.472 0.450
Table 3 The medium of the macular thickness
Central
Adenoid hypertrophy
Control
p value
241.38 ± 23.87
232.88 ± 20.37
0.054
significant difference was found between the two groups (p > 0.05) (Table 3).
Discussion Adenoid hypertrophy leads to the partial or total obstruction of the upper airway and is an independent risk factor of sleep-related disorder breathing ranges from simple snoring to OSAS [14]. OSAS is characterized by recurrent hypoxia and decreased oxygen saturations [3, 5]. It was mentioned that in OSAS, recurrent hypoxia and reperfusion episodes lead to oxidative stress and increased inflammation, vascular endothelial injury, decreased responsiveness to vasodilator agents, activation in the sympathetic system and thus vascular dysregulation occurs [15]. In a metaanalysis, which has investigated the studies about the effect of severity of OSAS in adults on choroidal thickness, it was suggested that the occurence of vascular dysregulation in OSAS deteriorate the choroidal blood flow and decrease choroidal thickness [3]. In the metaanalysis of He et al., 784 eyes (558 in the OSAS group, 226 in normal controls) in seven case–control studies were evaluated. The relationship between mild, moderate and severe OSAS and CT was studied. As results, subfoveal choroidal thickness was found to be significantly lower than the control group in OSAS. In the severe OSAS, the decline in the CT was more pronounced. Choroidal blood flow was preserved in mild OSAS [3]. The metaanalysis suggested that patients with moderate and severe OSAS may have dominate sympathetic activity and decreased choroidal blood flow. In only one of the seven studies, no correlation was between the severity of OSAS and choroidal thickness [2]. In the study of Karaca et al., previously diagnosed patients were not included because of mixing effect of the treatment regimen over the results. They suggested that their newly diagnosed patients did not suffer from OSAS for many years and probably had healthy parasympathetic innervations and
thus the choroidal blood flow can be preserved in these patients [2]. In this study, we would like to investigate whether the similar effect might be possible in children with obstructive symptoms due to severe adenoid hypertrophy. Polysomnography is the gold standard method to assess the severity of obstruction [16]. While in adults, apnea and hypopnea can be defined with definitive statements, there are no precise criteria in children [5]. Also the usage of polysomnography in clinical practice for children is limited because of its difficulty to apply in children. Therefore, we evaluated children according to their physical findings, parental reports of nocturnal symptoms and nocturnal video recordings. We included the patients, which had grade 3 and 4 adenoid hypertrophy according to Cassano and et al. and severe obstructive symptoms requiring surgery [12]. The lack of accurate duration of the obstructive symptoms is the limitation of this study. In the present study, we evaluated the choroid in three regions (subfoveal, nasal and temporal) and retina in the macular center fovea using EDI-OCT non-invasively. Choroid is an essential structure for retinal health [2]. The vascular supply of macular centre fovea, whose photoreceptors has the highest oxygen consumption, is completely through choroid [6]. Thus, the choroid and retina in the macular fovea are the most affected areas from vascular dysregulations [6]. The findings of this study revealed that severe adenoid hypertrophy did not cause a significant difference in choroidal thickness and also macular center thickness. Since the duration of the obstructive symptoms in children were less than adults in proportion to age, the sympathetic and parasympathetic fibers terminating on the choroid may remain balanced and no significant effect on choroid thickness may be observed. Therefore, we suggest that the choroidal blood flow is preserved in children with obstructive symptoms. In the literature, there were also studies [16–18] researching the effect of OSAS on retinal nerve fiber layer (RFNL) thickness, which is an important parameter to detect early sign of glaucoma. Increased sympathetic activity due to hypoxia in OSAS patients was thought causing vasospams and optical nerve damage [16]. The study of Cinici et al. investigated the thickness of retinal nerve fiber layer (RNFL) in children with adenotonsillary hypertrophy (ATH) [16]. Cinici et al. evaluated RNFL thickness of 57 children with ATH and 31 healthy controls by OCT. The age of participants ranged between 6 and 12 ages. Patients were divided into two groups as mild and severe OSAS patients according to their OSA-18 survey. They found no statistically significant difference between children with ATH and control group in terms of RFNL thickness. Poor correlation was determined between OSA-18 survey scores and RNFL thickness (p > 0.005). A positive correlation was found between ages and RNFL (p
