Egyptian Journal of Chest Diseases and Tuberculosis (2014) 63, 663–669

The Egyptian Society of Chest Diseases and Tuberculosis

Egyptian Journal of Chest Diseases and Tuberculosis

www.elsevier.com/locate/ejcdtwww.sciencedirect.com

ORIGINAL ARTICLE

Effect of sleep related breathing disorders on

ocular function

* Corresponding author. Tel.: +20 1224474317.E-mail address: enas_elsayed73@yahoo.com (E.E. Mohamed).

Peer review under responsibility of The Egyptian Society of Chest

Diseases and Tuberculosis.

Production and hosting by Elsevier

0422-7638 ª 2014 The Egyptian Society of Chest Diseases and Tuberculosis. Production and hosting by Elsevier B.V.

http://dx.doi.org/10.1016/j.ejcdt.2014.02.010Open access under CC BY-NC-ND license.

Enas Elsayed Mohamed a,*, Tamer Hamdy Massoud b

a Chest Diseases Department, Faculty of Medicine, Alexandria University, Egyptb Ophthalmology Department, Faculty of Medicine, Alexandria University, Egypt

Received 2 February 2014; accepted 17 February 2014Available online 15 March 2014

KEYWORDS

Obstructive sleep apnea

hypopnea syndrome;

Ocular complications

Abstract Introduction: Sleep disorders are common and obstructive sleep apnea hypopnea syn-

drome (OSAHS) is the commonest. OSAHS is not commonly diagnosed by the ophthalmologist,

but it has many systemic and ocular complications.

Aim of the work: The aim of this study was to detect the effect of sleep related breathing disor-

ders on ocular function.

Patients and methods: Thirty patients with OSAHS were enrolled after obtaining informed con-

sents. Patients were subjected to full history taking, Epworth sleepiness scale, anthropometric data,

Mallampati score, clinical apnea score, sleep study and complete ocular examination.

Results: 4 patients had mild OSAHS (13.33%), 12 patients had moderate OSAHS (40%) and 14

patients had severe OSAHS (46.67%) two of them had sleep hypoventilation. 4 patients were free

from any ocular manifestations. In 26 patients one or more of the following ocular findings were

found: floppy eyelid syndrome (FES) was detected in 3 (10%) patients, glaucoma was diagnosed

in 5 (16.67%) patients, senile cataract was found in 3 (10%) patients, nonarteritic anterior ischemic

optic neuropathy (NAION) was detected in 4 (13.33%) patients, papilledema was diagnosed in 3

(10%) patients and 18 (60%) patients had dry eye manifestations.

In conclusion: The increased prevalence of ocular symptoms and signs in patients with OSAHS

indicates a need to increase awareness and establish close collaboration with the sleep physicians

with clear pathways for review of OSAHS patients by the ophthalmic services. We should study

the effect of treatment of OSAHS on the ocular manifestations.ª 2014 The Egyptian Society of Chest Diseases and Tuberculosis. Production and hosting by Elsevier

B.V. Open access under CC BY-NC-ND license.

Introduction

Sleep disorders are common and obstructive sleep apnea hypo-

pnea syndrome (OSAHS) is the commonest. Approximately90% of patients who have obesity hypoventilation syndrome(OHS) exhibit sleep-disordered breathing consisting of

obstructive apneas and hypopneas (apnea-hypopnea index

664 E.E. Mohamed, T.H. Massoud

[AHI] P 5/h), whereas the remaining 10% of patients whohave OHS have an AHI less than 5/h. OSAHS is a potentiallyserious sleep disorder characterized by recurrent episodes of

breathing cessation during sleep secondary to upper airwaycollapse. Complete apnea or partial hypopnea episodes canlast from 10 s or more and may occur up to hundreds of times

nightly. It is often accompanied with swings in heart rate, a de-crease in oxygen saturation, and brief electroencephalogramarousals. Sleep apnea is a disorder not commonly diagnosed

by the ophthalmologist, but it has many systemic and ocularcomplications [1].

Floppy eyelid syndrome (FES), first described in 1981 byCulbertson and Ostler, is characterized by elastic upper eyelids

that are easily everted with minimal lateral traction, associatedwith a papillary conjunctivitis of the upper palpebral conjunc-tiva. A weak tarsal plate allows the lid to fold upon itself with

ease [2]. Obesity may be a confounding factor in the associa-tion of FES and OSAHS as many patients with OSAHS sufferfrom obesity [3].

Both normal tension and primary open-angle glaucomahave been associated with sleep apnea. Theories of mechanisminclude: (1) impaired optic nerve head blood flow secondary to

episodes of apnea, (2) optic nerve vascular dysregulation sec-ondary to arteriosclerosis and variations in arterial blood pres-sure, and (3) episodes of hypoxia. As ocular blood flow hasbeen suggested as a mechanism in glaucoma [4].

Non-Arteritic Ischemic Optic Neuropathy (NAION), anischemic event may be secondary to impaired optic nerve headblood flow autoregulation from apnea. Optic nerve vascular

dysregulation may also be a result of variations in arterialblood pressure seen in OSA, which may be due to an imbal-ance between nitric oxide and endothelin. Additionally, direct

damage by periods of hypoxia likely plays a role [5,6].Bucci and Krohel first reported a case of papilledema in a

patient with OSAHS in 1988, who had surgical treatment cor-

recting his OSAHS which resolved his papilledema [7]. Since,then, numerous cases have been reported of patients foundto have papilledema and idiopathic intracranial hypertension.Many of these patients, however, have had normal opening

pressures on lumbar puncture. Correction of their OSAHSwith continuous positive airway pressure (CPAP) treatmenthad resolved the papilledema [8].

Patients with sleep apnea have increased levels of circulat-ing epinephrine and norepinephrine. With elevated levels ofcatecholamines, OSAHS has been hypothesized to be a direct

risk factor for central serous chorioretinopathy (CSCR) [9].Retinal vein occlusions may be associated with OSAHS as

theymay be secondary to a slow-down of blood flow circulationsecondary to hypoxemia and elevated nocturnal intracranial

pressure. Strictly acting on the retinal microcirculation, OSAHSmay directly have a causal effect on retinal vein occlusions [10].

CPAP administered through a nasal or face mask has re-

mained the mainstay of treatment in OSAHS since its adventin the 1980s. Non-specific behavioral measures such as weightloss, avoiding smoking, alcohol, and sedatives can impact on

symptoms’ control, but are inadequate for moderate to severedisease. Effect of these treatment measures on the ocular man-ifestations is less well documented, as most literature docu-

ments ocular changes at the time of diagnosis of the sleepdisorder [1,5]. Isolated case reports in the literature have sug-gested reversal of symptoms of FES accompanied with signif-icant weight loss [11] and initiation of CPAP [12]. More

recently, effects of CPAP on intraocular pressure and perfor-mance in visual field (VF) testing have been reported [13,14].In addition, leaking from the masks used with CPAP can cause

ocular irritation and even induce conjunctivitis [15,16].

Aim of the work

The aim of this study was to detect the effect of sleep relatedbreathing disorders on ocular function.

Subjects and methods

Study population and subjects

Thirty patients with documented obstructive sleep apneahypopnea syndrome, admitted to the chest department, Alex-

andria main university hospital were enrolled after obtaining

informed consents.

Study measurements

All patients were subjected to the following:

1. Full history taking including age, sex, smoking index andhistory of other diseases.

2. Epworth sleepiness scale [17].

3. Anthropometric data including: Body mass index (BMI),neck circumference (NC), and waist/hip ratio. BMI derivedfrom the weight and height using the formula (Quetelet’s

index = weight (kg)/height (m)2).4. Thorough clinical examination including: Mallampati

score, general examination and local chest examination to

exclude other chest diseases and exacerbation.5. Clinical apnea score [18].6. Sleep study: all patients were subjected to overnight poly-

somnogram using somoscreen plus RC combi 39 includingthe following channels:� Flow (Cannula &/or Thermistor).� Snore (Cannula &/or Mic).

� Thoracic Effort (RIP Option).� Abdominal Effort (RIP Option).� Oxygen saturation (Spo2).

� Plethysmogram.� Pulse Rate.� Electrocardiogram (ECG).

� Obstruction.� CPAP/BiPAP Pressure.� Periodic leg movement (PLM).

� Electroencephalogram (EEG) (Fig. 1).

Apneas and hypopneas were scored using criteria estab-lished by the American Academy of Sleep Medicine (2012) [19].

Score a respiratory event in adults as an apnea if both of thefollowing were met:

a. There is a drop in the peak signal excursion by P90% ofpre-event baseline using an oronasal thermal sensor.

b. The duration of theP90%drop in sensor signal isP10 s.

In 2012 the American Academy of Sleep Medicine (AASM)Sleep Apnea Definitions Task Force reviewed the rules for

Figure 1 Somoscreen plus RC combi 39 device applied to the patient.

Effect of sleep related breathing disorders onocular function 665

scoring respiratory events in 2007 and gave new definition forhypopnea.

Score a respiratory event as a hypopnea if all of the follow-ing were met:

a. The peak signal excursions drop by P30% of pre-eventbaseline using nasal pressure.

b. The duration of the P30% drop in signal excursions isP10 s.

c. There is P3% oxygen desaturation from pre-event base-

line or the event is associated with an arousal.

The following parameters were calculated:

� Apnea hypopnea index (AHI): AHI is the total number ofapnea and/or hypopnea per hour of sleep.� Baseline O2 saturation: it is the oxygen saturation at the

start of the study.� Mean O2 saturation: it is the mean value of oxygen satura-tion during the total sleep time.

� Minimal O2 saturation: it is the lowest oxygen saturationrecorded during the total sleep time.� Oxygen desaturation index (ODI): it is the total number of

desaturations by at least 3% from the previous tracing perhour of sleep and it is calculated by dividing the total num-ber of desaturations by at least 3% from the previous trac-ing over the total sleep time (hrs).

� T90%: it is the percentage of sleep time with oxygen satura-tion below 90%.� Hypoventilation: We examined the overnight oximetric

tracing to assess if there was hypoventilation. Hypoventila-tion was considered when there was a sustained decrease of

SpO2 as detected by the oximeter (sagging of the oximetrictracing). Oximeter is a reliable tool to detect hypoventila-

tion whenever the patient is on room air and not receivingany supplemental oxygen.

After the sleep study all patients were subjected to CPAP as

a therapy to be titrated by a follow up study.

7. Full ophthalmological assessment through:

� Ophthalmic history taking (patients suffering from anyprevious ocular problems were excluded from the study).

� Uncorrected visual acuity (UCVA) measurement.

� Manifest refraction (MR).� Best corrected visual acuity (BCVA) measurement.� Slit lamp biomicroscopic examination of the anterior s-

egment of the eye and the ocular surface.� Dilated fundus examination for assessment of the condi-

tion of the retina and the optic nerve head.� Intraocular pressure measurement by applanation

tonometry.� The following investigations were performed when

needed:

� Fluorescein angiography.� Visual field assessment.� Optical coherence tomography.

Statistical analysis

Statistical analysis was performed with Sigma Stat 2.0 (SystatSoftware Inc., Point Richmond, Calif) and SPSS 14 (SPSS,Chicago, Ill) for Windows.

Figure 2 Floppy eye lids.

666 E.E. Mohamed, T.H. Massoud

Results

This study was carried on 30 patients subjected to the sleepstudy; 19 males (63.33%) and 11 females (36.67%). The age

ranged from 36 to 75 years with a mean ± SD value of54.6 ± 9.3 years, 18 patients (60%) were current or formersmokers and the pack year index had a mean ± SD value of

36.1 ± 20.32, 20 patients (66.67%) were diabetic and 15 pa-tients (50%) had history of hypertension. Epworth sleepinessscale (ESS) showed that 24 patients out of 30 (80%) hadhypersomnolence with an ESS of 10/24 or more.

The BMI of the patients ranged from 26.34 to 55.53 kg/m2

with a mean ± SD value of 33.25 ± 6.71 kg/m2, 22 of them(73.33%) were obese with BMI P30 kg/m2 and 8 of them

(26.67%) were overweight with BMI P 25–29.9 kg/m2. Theneck circumference (NC) ranged from 36 to 43 cm with amean ± SD value of 38.1 ± 2.87 cm. The waist/hip ratio ran-

ged from 0.89 to 1.12 with a mean ± SD value of 1 ± 0.05.The Mallampati score ranged from 1 to 4 with a

mean ± SD value of 2.7 ± 0.87. The clinical apnea score ran-

ged from 0 to 5 with a mean ± SD value of 1.53 ± 1.22.Table (1) showed the polysomnographic respiratory data of

the studied patients, 4 patients had mild OSAHS (13.33%), 12patients had moderate OSAHS (40%) and 14 patients had se-

vere OSAHS (46.67%) two of them had sleep hypoventilation.Table (2) showed the ocular findings of the studied patients;

4 patients were free from any ocular manifestations (patients

with mild OSAHS). In 26 patients (patients with moderateand severe OSAHS) one or more of the following findings werefound: floppy eyelid syndrome (FES) was detected in 3 (10%)

Table 1 Data of the sleep study.

The sleep parameters Mean ± SD

Apnea/hypopnea index 65 ± 29.75/h

Basal oxygen saturation 91.73 ± 4.90%

Mean oxygen saturation 83.95 ± 7.59%

Minimal oxygen saturation 61.62 ± 18.74%

Oxygen desaturation index (ODI) 49.78 ± 22.32/h

T90% 3.46 ± 1.21% of the total

sleep time

Table 2 Data of the ocular findings.

The ocular findings Number and

percentage of

patients

Floppy eyelid syndrome (FES) (n= 3) 10%

Glaucoma (n= 5) 16.67%

Senile cataract (n= 3) 10%

Non-arteritic ischemic optic neuropathy

(NAION)

(n= 4) 13.33%

Papilledema (n= 3) 10%

Dry eye manifestations [in the form of

conjunctival hyperaemia, lid parallel

conjunctival folds and conjunctivo-chalasis

(redundant conjunctiva)]

(n= 18) 60%

Free from any ocular manifestations (n= 4) 13.33%

Figure 3 Glaucomatous optic disc cupping.

patients, glaucoma was diagnosed in 5 (16.67%) patients, se-nile cataract was found in 3 (10%) patients, nonarteritic ante-

rior ischemic optic neuropathy (NAION) was detected in 4(13.33%) patients, papilledema was diagnosed in 3 (10%) pa-tients and 18 (60%) patients had dry eye manifestations [in the

form of conjunctival hyperaemia, lid parallel conjunctivalfolds and conjunctivo-chalasis (redundant conjunctiva)](Figs. 2–5).

Figure 4 Conjunctival Hyperaemia.

Figure 5 Redundant Conjunctiva.

Effect of sleep related breathing disorders onocular function 667

Discussion

OSAHS is associated with a number of serious systemic dis-eases and also several eye disorders including floppy eyelid syn-

drome, optic neuropathy, glaucoma, anterior ischemic opticneuropathy and papilledema secondary to raised intracranialpressure. Treatment of OSAHS may help floppy eyelid syn-

drome, stop progression of associated glaucoma, and reduceintracranial pressure in patients with associated papilledema.The diagnosis of OSAHS can only be made with formal sleepstudies, but asking a small number of appropriate questions

will help screen those patients who should be referred to sleepstudies [5].

In this study, all patients with mild OSAHS were free from

any ocular manifestations and ocular manifestations existed inpatients with moderate and severe OSAHS. Floppy eyelid syn-drome (FES) was detected in 3 (10%) patients with OSAHS.

FFS is one of the ocular disorders that have been associatedwith OSAHS. It is characterized by rubbery, redundant uppereyelid tissue and papillary conjunctivitis, and is seen most com-

monly in obese middle-aged men. The affected eyelid may cor-respond to the side on which the patient prefers to sleep. Theetiology is uncertain, but current theories include an upregula-tion of elastin-degrading matrix metalloproteinases possibly

caused by direct eyelid trauma, ischemia–reperfusion injury

due to pressure placed on the eyelid, or low arterial oxygentension during sleep; again obesity is a risk factor for bothFES and OSAHS. When FES is severe, the eyelid may sponta-

neously evert during sleep and rub on the patient’s pillow,causing an acute exacerbation of mechanically induced con-junctivitis. The prevalence of OSAHS in patients with FES

has been reported to be as high as 90 percent; only 2–5 percentof patients with OSAHS may have FES. Thus, it is impracticalto screen all patients with OSAHS for FES. However, all

patients with FES who do not have an established diagnosisof OSAHS should have a thorough sleep history taken and,when appropriate, should be referred to sleep evaluationincluding polysomnography. Patients with FES and OSAHS

who are already being treated with CPAP need to have theirmasks properly fitted to avoid additional eye injury due to mis-directed air further drying out the eyes [20].

The range of reported rates of FES prevalence (2.3–32%) indifferent series of OSAHS patients includes Karger et al. [21],1/44, 2.3%; Roberts et al. [22], 1/46, 2.2%; McNab [23], 3/20,

15%; and in 1999 Mojon et al. [24], found 14/44 (32%) pa-tients with OSAHS had FES. All, but one of the studies (i.e.Robert et al. [22]), were conducted at the time of initial referral

to OSAHS before initiation of CPAP.In the current study, glaucoma was diagnosed in 5

(16.67%) patients; the link between glaucoma and OSAHS iscontroversial. There was a high prevalence of both primary

open-angle glaucoma and normal-tension glaucoma amongpatients with OSAH. Several studies have identified OSAHSin patients with glaucomatous optic disc cupping and associ-

ated visual field defects who do not respond to medical or sur-gical intraocular pressure lowering treatments, but whosevisual fields stabilize when treated with CPAP [4,5]. One

Chinese study showed that patients with OSAHS were fourtimes more likely to have glaucomatous optic disc changesand visual field defects than age-matched controls [25].

Another study by Mojon et al. [4] reported the prevalenceof glaucoma among 69 patients with obstructive sleep apneato be 7.2%. Waller et al. [26] criticized the design of manystudies looking for a relationship between glaucoma and

obstructive sleep apnea. Their criticisms included flawed fromreliance on reported symptoms, lack of properly matched con-trols, etc. In Waller et al’s study of 100 patients with obstruc-

tive sleep apnea, they found the prevalence of glaucoma to be27%. Based on Mojon and Waller’s reports, the most cautiousapproach would be to have all obstructive sleep apnea patients

screened for glaucoma, and OSAHS should be considered as apossibility in all patients with primary open angle or normaltension glaucoma.

In the present study, nonarteritic anterior ischemic optic

neuropathy (NAION) was detected in 4 (13.33%) patients.The prevalence of obstructive sleep apnea among those withNAION has been reported at 71–89%. The prevalence of

NAION among those with OSA has not been studied. Thepossible causal relationship between OSAHS and NAION isvery similar to their list of possible mechanisms relating glau-

coma and obstructive sleep apnea [5].In 2002 Mojon et al. [27] proposed mechanisms for nonarte-

ritic anterior ischemic optic neuropathy in patients with

obstructive sleep apnea include the following: obstructive sleepapnea results in impaired vascular autoregulation of the opticnerve’s circulation; obstructive sleep apnea induces arterioscle-rosis and arterial hypertension, which in turn induce optic nerve

668 E.E. Mohamed, T.H. Massoud

vascular ‘‘dysregulation’’; repetitive hypoxia directly damagesthe optic nerve; obstructive sleep apnea causes an imbalance be-tween nitric oxide and endothelin (vasodilatory and vasocon-

strictive factors). Palombi et al. [28] had noted an even higherprevalence in their study where 89% of patients with NAIONhad sleep apnea. It has been suggested that patients with

NAION can be questioned about their sleep habits. One re-search group that did this elicited a history of OSAHS 2.5 timesmore often in patients with NAION than in controls [29].

In this study, papilledema was diagnosed in 3 (10%)patients. Papilledema also associated with OSAHS, is thoughtto be caused by nocturnal increase in intracranial pressure.Potential mechanisms include raised venous pressure due to

forced inspiration against a closed airway or hypoxia-inducedcerebral venous dilation. When neuroimaging is normal, acareful sleep history in a patient with papilledema is critical

in order to determine whether OSAHS is a causative factor.In such patients, treatment of the OSAHS has been shownto improve, resolve or halt the progression of papilledema [5].

Sugita et al. [30] did 24-h monitoring of intracranial pres-sure in patients with obstructive sleep apnea. Sugita et al. foundthat intracranial pressure increases during sleep in association

with apnea, and the longer the duration of the apnea, the great-er the increase in ICP. Episodes of apnea would ‘‘precede andaccompany’’ episodes of intracranial pressure increase. Noneof their patients had increased intracranial in the daytime.

Sugita et al. hypothesized that the dull morning headaches thatare common in those with obstructive sleep apnea may beattributable to ceresbrospinal fluid pressure increase during

sleep. Waller et al. [26] said that some patients with more severeobstructive sleep apnea have low blood oxygen levels and in-creased intracranial pressure even in the daytime.

Purvin et al. [31] studied four patients with obstructive sleepapnea and papilledema. Purvin et al. hypothesized that lowblood oxygen and high CO2 would cause cerebral vasodilation,

which in turn would result in transient increase in intracranialpressure.

In the present study, 18 (60%) patients had dry eye mani-festations in the form of chronic conjunctival hyperaemia, lid

parallel conjunctival folds and conjunctivo-chalasis (redun-dant conjunctiva). A variety of common ocular surface prob-lems have been associated with CPAP use which delivers air

under pressure to the nose.Leaks from the CPAP mask hitting the face and eyes are

the main cause for dry eyes. Fixing these leaks can eliminate

these dry eyes. When the patient starts to put the CPAP maskon, it is very important to let the mask loose on the face andthen start the CPAP machine. In this way, the mask cushionwill fill up with air. Then the patient can tighten the straps

on the face. If the leaks could not stop, we should changethe mask or use special goggles to protect the eyes from theair blowing in them.

Some patients with sleep apnea have problems with the tearducts, sinuses and eyelids. The air that enters in the airwaysfrom the CPAP could also enter through these ducts to the

eyes. If the air from the CPAP machine is also humidified,the liquid may accumulate under the skin around the eyes [24].

During the night, air may escape from around the mask and

blow onto the eyes resulting in morning sensations of dry, irri-tated eyes and conjunctivitis, alternatively air may find its wayup through the nasolacrimal duct, and cause similar problems.There are a series of valves that guard against retrograde flow

up the duct, but in many people these valves are not totallyeffective in preventing retrograde flow [15]. Therefore theinvestigators try to find other methods of treatment of OSAHS

and their findings establish proof-of-principle that targetedblockade of certain potassium channels at the hypoglossal mo-tor pool is an effective strategy for reversing upper airway

hypotonia and causing sustained reactivation of genioglossusthroughout non rapid eye movement and rapid eye movementsleep. These findings identify an important new direction for

translational approaches to the pharmacological treatment ofobstructive sleep apnea [32].

In conclusion, the increased prevalence of ocular symptomsand signs in patients with OSAHS indicates a need to increase

awareness and establish close collaboration with the sleep phy-sicians with clear pathways for review of OSAHS patients bythe ophthalmic services. We should study the effect of treat-

ment of OSAHS with CPAP on the ocular manifestations.

Conflict of interest

The authors declare no conflict of interest.

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