Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

The Effects of Surgical Treatment on Retina-Choroidal Findings in Patients With Obstructive Sleep Apnea Syndrome

Hüseyin Kaya, MD; Gökhan Pekel, MD; Derya Kaya, MD; Cüneyt Orhan Kara, MD; Mehmet Can Hıraali, MD

Abstract

BACKGROUND AND OBJECTIVE:

The purpose of this study was to determine the effect of surgical treatment on ocular findings in obstructive sleep apnea syndrome (OSAS).

PATIENTS AND METHODS:

The authors studied 34 eyes of 34 newly diagnosed OSAS patients. The sleep study was performed before and 6 months after expansion sphincter pharyngoplasty (ESP). Retinal nerve fiber layer (RNFL), choroidal thickness (CT), and retinal arteriolar caliber (RAC) analyses were performed using spectral-domain optical coherence tomography. Intraocular pressure (IOP) and ocular pulse amplitude were performed using the Pascal dynamic contour tonometer.

RESULTS:

The preoperative and postoperative Apnea Hypopnea Index scores and average oxygen saturation values were significantly different (P = .0001 and P = .001, respectively). There was no significant difference between the preoperative and postoperative RNFL thicknesses (P > .05). The preoperative subfoveal, nasal, temporal CT, and IOP were significantly different from the postoperative measurements (P = .006, P = .05, P = .036, and P = .0001, respectively).

CONCLUSIONS:

ESP had a significant influence on CT and IOP in patients with OSAS, maintaining a decrease in CT and IOP 6 months after surgery. The determination of these ocular findings may be useful to show the positive effects of ESP.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:35–42.]

Abstract

BACKGROUND AND OBJECTIVE:

The purpose of this study was to determine the effect of surgical treatment on ocular findings in obstructive sleep apnea syndrome (OSAS).

PATIENTS AND METHODS:

The authors studied 34 eyes of 34 newly diagnosed OSAS patients. The sleep study was performed before and 6 months after expansion sphincter pharyngoplasty (ESP). Retinal nerve fiber layer (RNFL), choroidal thickness (CT), and retinal arteriolar caliber (RAC) analyses were performed using spectral-domain optical coherence tomography. Intraocular pressure (IOP) and ocular pulse amplitude were performed using the Pascal dynamic contour tonometer.

RESULTS:

The preoperative and postoperative Apnea Hypopnea Index scores and average oxygen saturation values were significantly different (P = .0001 and P = .001, respectively). There was no significant difference between the preoperative and postoperative RNFL thicknesses (P > .05). The preoperative subfoveal, nasal, temporal CT, and IOP were significantly different from the postoperative measurements (P = .006, P = .05, P = .036, and P = .0001, respectively).

CONCLUSIONS:

ESP had a significant influence on CT and IOP in patients with OSAS, maintaining a decrease in CT and IOP 6 months after surgery. The determination of these ocular findings may be useful to show the positive effects of ESP.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:35–42.]

Introduction

Obstructive sleep apnea syndrome (OSAS) is a disorder characterized by recurrent episodes of complete or partial upper airway obstruction during sleep. The prevalence of OSAS is 2% to 5% in the middle-aged population. Obesity, being male, thick neck, abnormality of the upper respiratory tract, alcohol abuse, and snoring are certain risk factors for OSAS.1 OSAS is diagnosed by overnight polysomnography.2

OSAS is associated with several ophthalmic disorders, including glaucoma, nonarteritic anterior ischemic optic neuropathy, optic disc edema, central serous chorioretinopathy, and retinal vein occlusions.3–8 The increased risk of glaucoma in OSAS patients has been reported in several studies.3,9 Inflammatory processes, oxidative stress, endothelial dysfunction, and vascular remodeling may play roles in the pathogenesis of vascular complications in OSAS.10,11 These changes may influence the optic nerve head perfusion and may result in ganglion cell loss. Concordantly, decreased retinal nerve fiber layer (RNFL) thickness and increased optic nerve head area-volume parameters measured with optical coherence tomography (OCT) have been reported in patients with OSAS in recent studies.12,13 OCT is also an effective technology for evaluating choroidal thickness (CT) and retinal arteriolar caliber (RAC).14,15

The dynamic contour tonometry is a noninvasive measuring device that accurately measures (independent of the thickness or elasticity of cornea) the intraocular pressure (IOP) and ocular pulse amplitude (OPA).16,17 Choroidal circulation has an important role in ocular physiology and may also be affected by several ocular and systemic diseases.18,19 OPA is accepted as an indirect measurement of choroidal blood flow such that it provides insight into the choroidal circulation.16,17

The collapsibility of the upper airway during sleep is the essential cause of obstructive sleep apnea. When these collapsible soft tissues are exposed to negative pressure within the upper airway, complete or partial obstruction of the upper airway may cause the interruption of breathing, increased blood pressure, and hypoxemia.20 For the treatment of this collapse, different surgical procedures were described.21–23 Expansion sphincter pharyngoplasty (ESP) is one of these procedures with high success rate and minimal morbidity.24

There has been little investigation of patients with OSAS before and after ESP operation according to ocular findings. This study was intended to evaluate the difference between the preoperative and postoperative values of CT, OPA, IOP, RAC, and the RNFL. We aimed to find possible benefits of surgical treatment on ocular findings, especially RNFL thickness and choroidal circulation, in patients with OSAS.

Patients and Methods

This comparative study involved 34 eyes of 34 (30 male and four female) newly-diagnosed OSAS patients. The institutional board for ethics approved the study and adhered to the standards of the Declaration of Helsinki. Informed consent was obtained from every subject participating in the study. All measurements (polysomnographic study, CT, RNFL, RAC, OPA, IOP) were taken before and 6 months after the operation.

After the polysomnographic study, patients with an AHI greater than or equal to 5 were considered to have OSAS. Overnight polysomnography was performed in all subjects using a computerized system (Somnologica software; Ferguson Medical, Sikeston, MO). Apneas were characterized as complete cessation of airflow for longer than 10 seconds. Hypopneas were characterized as a 50% or higher reduction in airflow signal with a fall of more than 3% in oxygen saturation or an arousal. The AHI was computed by dividing the number of apneas and hypopneas by sleep time. Patients were classified according to AHI. Those with an AHI value of 5 to 15 were considered mild (13 patients); those registering between 16 and 30 were considered moderate (12 patients), and those over 30 were considered severe (nine patients) OSAS patients.25 The average oxygen saturation during sleep was calculated during the polysomnographic study. After the diagnosis was made by polysomnography, ESP was performed as a surgical method. ESP is a surgical technique first defined in 2007 by Pang and Woodson.21 The surgical procedure was described as essentially a bilateral tonsillectomy, a palatopharyngeus muscle rotation flap that is antero-superolaterally rotated through the muscle mass itself with a vicryl 4/0 suture.21

The RNFL, RAC, and CT analyses were performed using the spectral-domain OCT (SD-OCT) (Spectralis software version 5.8; Heidelberg Engineering, Heidelberg, Germany). The same physician (HK) performed the measurements between the hours of 8:30 a.m. and 9:30 a.m. before and 6 months after the operation. The measurements were repeated three times, and the best quality images were selected. Two blind expert and experienced ophthalmologists (MCH and GP) measured the images for correct reading. The CT was measured straightly using manual caliber tools (Spectralis software) from the outer border of the hyperreflective retinal pigment epithelium to the inner sclera. The CT was measured at the fovea and at 1 mm temporal and 1 mm nasal to the fovea, as shown in Figure 1. The RAC was measured by the manual caliber supplied by the Spectralis software on the peripapillary RNFL analysis screen. The three largest retinal arterioles passing through an area of 1 disc diameter from the optic disc margin were measured (Figure 2). The measurements were performed with a magnification of approximately 250% to detect borders of arterioles more accurately. The mean thickness values of retinal arterioles were calculated for each patient and recorded for analysis. The average RNFL thickness and the four-quadrant (inferior, superior, temporal, and nasal) RNFL thickness were described in microns (μm) (Figure 3).

Optical coherence tomography scan showing the choroidal thickness (CT). CT was measured perpendicularly from the outer edge of the hyperreflective retinal pigment epithelium to the inner sclera at the fovea and at 1 mm temporal and 1 mm nasal to the fovea.

Figure 1.

Optical coherence tomography scan showing the choroidal thickness (CT). CT was measured perpendicularly from the outer edge of the hyperreflective retinal pigment epithelium to the inner sclera at the fovea and at 1 mm temporal and 1 mm nasal to the fovea.

The retinal arteriolar caliber measurement by the manual caliber supplied by the Spectralis software (Heidelberg Engineering, Heidelberg, Germany) on the peripapillary retinal nerve fiber layer analysis screen. The three largest retinal arterioles passing through an area of 1 disc diameter from the optic disc margin were measured.

Figure 2.

The retinal arteriolar caliber measurement by the manual caliber supplied by the Spectralis software (Heidelberg Engineering, Heidelberg, Germany) on the peripapillary retinal nerve fiber layer analysis screen. The three largest retinal arterioles passing through an area of 1 disc diameter from the optic disc margin were measured.

The retinal nerve fiber layer thickness screen.

Figure 3.

The retinal nerve fiber layer thickness screen.

Patients with any known systemic diseases other than OSAS like diabetes mellitus, cardiovascular disease, systemic arterial hypertension; any eye diseases like retinal or choroidal diseases, glaucoma, ocular trauma or surgery, ocular inflammation, and refractive errors outside −1.5 to +1.5 D were excluded. Taking medication and smoking were also considered exclusion criteria.

OPA and IOP measurements were practiced using the Pascal dynamic contour tonometer (Pascal DCT; Swiss Microtechnology AG, Port, Switzerland). This is a slit-lamp biomicroscopy mounted, self-calibrating, 7-mm tip diameter, and 1.2-mm pressure sensor diameter device. One drop of Alcaine (proparacaine chloride 5 mg/mL; Alcon, Fort Worth, TX) was instilled just before IOP and OPA measurements, which were taken in triplicate for each eye in order to obtain one good-quality measurement. Only quality 1 and 2 measurements were considered. The same investigator (HK) performed all OPA and IOP measurements.

The statistical package SPSS 21.0 for Windows (IBM, Armonk, NY) was used to perform the statistical analysis. Continuous data were reported as mean ± standard deviation and median (min – max values). Shapiro–Wilk tests was used for testing normality. If parametric test conditions were satisfied, one-way analysis of variance (ANOVA) was used for comparisons among groups. The post-hoc Tukey test was used when the ANOVA determined a significant difference. If parametric test conditions were not satisfied, the Kruskal–Wallis Variance Analysis was used for comparisons among groups. The post-hoc Mann Whitney U-Test with Bonferroni Correction was used when the Kruskal Wallis Variance Analysis determined a significant difference. If parametric test conditions were satisfied, paired samples t-test was used for comparing dependent groups. If parametric test conditions were not satisfied, Wilcoxon test was used for comparing dependent groups.

Results

This study included 34 newly diagnosed OSAS patients. The average age of the patients was 43.94 years ± 9.89 years. Table 1 shows the patients' BMI, AHI, and oxygen saturation (SpO2) values during sleep. The preoperative and postoperative AHI scores and average SpO2 are significantly different (P = .0001 and P = .001, respectively) (Table 1).

Preoperative and Postoperative Mean AHI Scores, BMI, SpO2 Saturations, and P Values of the Patients With Sleep Apnea Syndrome

Table 1:

Preoperative and Postoperative Mean AHI Scores, BMI, SpO2 Saturations, and P Values of the Patients With Sleep Apnea Syndrome

Table 2 shows the comparisons of the preoperative and postoperative RNFL thickness in patients with OSAS. There was no significant difference between preoperative and postoperative measurements (P > .05) (Table 2).

Mean Preoperative and Postoperative RNFL Thickness Values (μm)

Table 2:

Mean Preoperative and Postoperative RNFL Thickness Values (μm)

Table 3 shows the comparisons of the preoperative and postoperative subfoveal, nasal, and temporal CT values. The preoperative subfoveal, nasal, and temporal CT measurements were 287.68 μm ± 57.09 μm, 276.03 μm ± 51.42 μm, and 287.97 μm ± 56.03 μm, respectively, and the postoperative measurements were 274.68 μm ± 57.24 μm, 269.94 μm ± 53.5 μm, and 276.38 μm ± 54.06 μm, respectively. The differences were statistically significant (P = .006, P = .05, and P = .036, respectively) (Table 3.).

Mean Preoperative and Postoperative Subfoveal, Nasal, and TemporalChoroidal Thickness (μm)

Table 3:

Mean Preoperative and Postoperative Subfoveal, Nasal, and TemporalChoroidal Thickness (μm)

Table 4 shows the comparisons of the preoperative and postoperative IOP, OPA, and RAC values. The postoperative mean IOP measurement was lower than the preoperative IOP, and the difference was statistically significant (P = .0001). The difference between the preoperative and postoperative OPA and retinal arteriole caliber (RAC) measurements were not statistically significant (P = .75 and P = .10) (Table 4.).

Mean Preoperative and Postoperative IOP, OPA, and RAC Values

Table 4:

Mean Preoperative and Postoperative IOP, OPA, and RAC Values

Discussion

In our study, significant differences between preoperative and postoperative CT and IOP were observed. Additionally, SpO2 and AHI scores were significantly different after ESP surgery. According to these results, we think that ESP is an effective method in the treatment of sleep apnea but also shows an improvement in the ocular findings.

Intermittent airway obstruction causes hypoxia in OSAS patients and a decrease in the main saturation of oxygen. Hypoxemia causes an increase in the levels of the vasoconstrictor endothelin generation and a decrease in the levels of vasodilator nitric oxide generation. This condition can lead to an increase in vascular resistance. The endothelial cells can also produce a vasodilator agent, nitric oxide.26,27 In OSAS, the equilibrium between endothelium-mediated vasoconstrictor and vasodilator is noticeably impaired, such that the vasodilator response crucially decreased. Additionally, hypoxemia can lead to activation of the adrenergic system, high sympathetic tone, and elevated muscle sympathetic nerve activity.11 All of these conditions may cause ganglion cell loss leading to optic disc damage.26,27 Some studies have reported that the RNFL thickness in patients with OSAS was significantly thinner than in control groups.28,12 The severity of OSAS may also be an important factor for RNFL thickness. Kargı et al. and Lin et al. reported that the severity of OSAS and the RNFL thickness were significantly correlated.28 On the other hand, other studies have reported no significant correlation.13,29

This study aimed to show the effect of treatment on RNFL, CT, IOP, RAC, and OPA. In our study, the RNFL thicknesses of all groups did not change significantly between preoperative and postoperative measurements. Shiba et al. reported a significant negative correlation between the AHI and the nasal RNFL thickness.30 According to this study, the severity of OSAS may generate unique retinal neurodegenerative disorders. This may be responsible for the nasal RNFL thickness decrease.30 They also said that further investigation is needed to confirm whether treatment of OSAS prevents decreases in the RNFL thickness.30 In the current study, the mean preoperative and postoperative AHI scores were 20.19 and 11.08, respectively. The difference was statistically significant. Reduction in AHI score could avoid thinning of the RNFL thickness. The postoperative average SpO2 value (95.03%) was also found to be higher than preoperative average SpO2 values (94.03%). The increase of the average SpO2 may have protected the ganglion cells from the adverse effects of hypoxia.

Some studies have shown an increased risk of glaucoma in the OSAS population.3,9 Chen et al. conducted a population-based retrospective cohort study on 2,528 patients with OSAS and 10,112 without OSAS.31 They showed that pharyngeal and nasal surgery for OSAS both effectively reduced the risk of glaucoma, although pharyngeal surgery was found to be more effective than nasal surgery. The authors also found that only continuous positive airway pressure (CPAP) treatment could not reduce the risk of glaucoma in OSAS.31 In the current study, the postoperative IOP was significantly lower than the preoperative IOP significantly. The OPA did not differ significantly between the preoperative and postoperative measurements. The decrement of IOP also (in addition to decrement in postoperative AHI scores and increase in postoperative average SpO2) may help protect ganglion cells from damage.

Xin et al. showed decreased foveal and nasal macular thickness, similar to the subfoveal and nasal CT in OSAS patients, suggesting that OSAS might change the retinal and choroidal blood supply because of intermittent hypoxia.32 Bayhan et al. observed that OSAS patients had thinner CT nasal to the fovea, and nasal CT of OSAS patients negatively correlated with AHI.33 In contrast to these studies, Tonini et al. showed unimpaired choroidal vascular reactivity in 16 patients with OSAS without comorbidities using laser Doppler flowmetry.34 They showed that the absence of comorbidities might be the main reason for the similar choroidal vascular responses in OSAS and controls. The authors also concluded that changes might be more significant in more severely affected patients with longer disease duration or those with comorbidities. In addition, the authors hypothesize that the choroid is protected against low or moderate OSAS by long-term adaptive mechanisms.34

In our study, the postoperative mean subfoveal, nasal, and temporal CT were found to be thinner than the preoperative measurements (P = .006, P = .05, and P = .036, respectively). As a result of surgery, reduction in AHI scores and increased average SpO2 might have prevented the bad effects of hypoxia-like impaired equilibrium between vasoconstrictor and vasodilator mechanisms.11 The decrease in CT may be an adaptation to increased SpO2 or decreased AHI scores and IOP after surgery. Du et al. investigated the changes of retinal SpO2 concentrations, CT, and RNFL in eyes with acute primary angle closure at 1 day and 1 month after trabeculectomy.35 The mean retinal oxygen saturation was found increased 1 month after trabeculectomy and the average CT became thinner 1 month after surgery. According to the results of this study, larger CT could be a protective mechanism against the ischemia and CT decreased to normal with IOP decline.

A recently developed sleep endoscopy technique and Müller maneuver with flexible nasopharyngoscopy have shown that lateral pharyngeal wall collapse is important in the pathogenesis of OSAS patients.36 The aim of OSAS surgery is to expand the anatomical region causing collapse.24 The selection of the case group in this study was made by Müller maneuver by flexible nasopharyngoscopy and sleep endoscopy in the operating room. Patients with collapsed lateral pharyngeal wall level at sleep endoscopy were included in this study.

ESP operation is a relatively new surgical method than the others. For this reason, there are few patients in the previous studies about ESP. ESP is recommended for patients with collapse of the lateral pharyngeal wall. ESP is also superior to conventional surgical methods to repair collapse of the lateral pharyngeal wall.22 Although ESP is an effective method in mild and moderate OSAS patients, it is also useful in lowering the AHI score in severe OSAS patients. The preoperative and postoperative AHI values in our study are consistent with many recent studies investigating the success of the ESP method.37,38 The main objective in all of the OSAS surgeries is to reduce the AHI score.22,36,37 Reducing the AHI score increases SpO2. Therefore, we think that OSAS surgeries other than ESP method may affect eye findings positively. We think that more studies are needed to generalize the results of our study. However, we think that the results of our study will be a basis for future studies.

The current study had some limitations. First, we do not know how long our patients suffered from OSAS before their clinical diagnosis; choroidal alterations may occur gradually or intermittently over long periods of time with the disease. Second, we examined the patients only two times: before the operation and 6 months after the operation. If the follow-up period was longer, the results might be more significant.

In conclusion, the CT and IOP measurements were decreased after ESP significantly. AHI scores were decreased significantly after operation. Also SpO2 levels were significantly increased after ESP. According to these results, the study showed the possible preventive effect of ESP on ocular findings in OSAS patients. We think that the treatment of OSAS patients by ESP without delay may improve on ocular findings. Further studies should be performed on the effect of surgical treatment on glaucomatous findings and CT in this group of patients.

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Preoperative and Postoperative Mean AHI Scores, BMI, SpO2 Saturations, and P Values of the Patients With Sleep Apnea Syndrome

PreoperativePostoperativeP Value
AHI20.19 ± 12.8611.08 ± 10.72.0001*
SpO2%94.03 ± 1.9595.03 ± 1.14.001*
BMI29.02 ± 2.5828.9 ± 2.83.569

Mean Preoperative and Postoperative RNFL Thickness Values (μm)

PreoperativePostoperativeP Value
Average103.97 ± 9103 ± 8.25.772
Superior125.15 ± 15.9125.42 ± 15.87.59
Inferior138.42 ± 18.11138.71 ± 18.47.221
Temporal77.59 ± 17.175.21 ± 11.84.324
Nasal76.82 ± 14.7375.59 ± 11.36.382

Mean Preoperative and Postoperative Subfoveal, Nasal, and TemporalChoroidal Thickness (μm)

PreoperativePostoperativeP Value
Subfoveal287.68 ± 57.09274.68 ± 57.24.006*
Nasal276.03 ± 51.42269.94 ± 53.5.05*
Temporal287.97 ± 56.03276.38 ± 54.06.036*

Mean Preoperative and Postoperative IOP, OPA, and RAC Values

PreoperativePostoperativeP Value
IOP18.57 ± 2.6616.93 ± 3.07.0001*
OPA2.05 ± 0.662.04 ± 0.58.759
RAC87.29 ± 8.788.9 ± 7.42.106
Authors

From Pamukkale University, Ophthalmology Department, Denizli, Turkey (HK, GP); the Department of Otolaryngology — Head and Neck Surgery, Servergazi State Hospital, Denizli, Turkey (DK); the Department of Otolaryngology — Head and Neck Surgery, Pamukkale University, Denizli, Turkey (COK); and Kilis State Hospital, Ophthalmology Clinic, Kilis, Turkey (MCH).

The authors report no relevant financial disclosures.

Address correspondence to Hüseyin Kaya, MD, Pamukkale University, Ophthalmology Department, Denizli, Turkey 20070; email: hsynkaya@gmail.com.

Received: December 11, 2018
Accepted: July 29, 2019

10.3928/23258160-20191211-05

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