ORIGINAL STUDY

Meta-Analysis of Association of Obstructive Sleep Apnea

With Glaucoma
Shulin Liu, MD,* Yu Lin, BS,w and Xin Liu, BSz

Objectives: Previous studies suggested that obstructive sleep apnea

(OSA) was associated with glaucoma. However, data on this issue
are controversial. This study aims to use meta-analysis to determine whether OSA is related to glaucoma.
Materials and Methods: We searched PubMed, Embase, the
Cochrane library, the Web of Science, and the Chinese BioMedical
Literature Database disk databases up to November 20, 2014 for
related literature. The association of OSA with glaucoma was
assessed by odds ratio (OR) with 95% condence interval (CI) as
the eect size. Then subgroup analysis was performed according to
area and glaucoma type.
Results: Six primary studies (3 cohort study and 3 case-control
studies) were included in this meta-analysis involving 2,288,701
participants. There was a signicant association between OSA and
glaucoma (adjusted-eect summary for case-control studies
OR = 2.46; 95% CI, 1.32-4.59, P = 0.005) (adjusted-eect summary for cohort studies OR = 1.43; 95% CI, 1.21-1.69, P = 0.000).
There was no signicant publication bias.
Conclusion: OSA was a risk factor for glaucoma. A large number of
studies is needed to explore the mechanisms that link OSA with
glaucoma.
Key Words: obstructive sleep apnea, glaucoma, meta-analysis

(J Glaucoma 2016;25:17)

Obstructive sleep apnea (OSA) is a common disorder

characterized by repetitive complete or partial obstruction
of the upper airway during sleep causing nocturnal recurrent oxygen desaturations. OSA will cause hypoxia,
hypercapnea, increased vascular resistance, and sympathetic activation.2,3 Polysomnography can be used to
diagnose OSA, a score of Z5 is required in the apnea
hypopnea index. Continuous positive airway pressure
(CPAP) is the standard therapy to prevent upper airway
collapse. However, CPAP can increase intraocular pressure.4 The prevalence of OSA is 2% to 4% in males and 1%
to 2% in females,5,6 and is higher in Asians.7 Previous
studies have suggested that OSA was associated with several eye disorders, including oppy eyelid syndrome, conjunctivitis, keratitis, keratoconus, papilledema, and optic
neuropathy.8,9 Studies also showed that people with OSA
had a higher risk for glaucoma compared with normal
people.1013 On the contrary, it is also reported that OSA
did not increase the risk of glaucoma.1418 It is dicult to
draw conclusions from the current literature and there are
no reports of meta-analysis on their association. To address
these concerns, we performed a meta-analysis of cohort and
case-control studies to examine the risk of glaucoma
between people with and without OSA.

MATERIALS AND METHODS

laucoma is dened as a chronic progressive optic neuropathy and is the second leading cause of blindness worldwide. There are many dierent types of glaucoma, such as
congenital glaucoma, open-angle glaucoma (OAG), normaltension glaucoma (NTG), and angle-closure glaucoma (ACG).
The number of people aected by the disease will increase to an
estimation of 79.6 million in the year 2020.1 Although a number
of risk factors associated with the development of glaucoma
have been identied, the etiology of this disease remains unclear.
Received for publication February 26, 2015; accepted October 11, 2015.
From the *Chongqing Key Laboratory of Ophthalmology, Chongqing
Eye Institute, The First Aliated Hospital of Chongqing Medical
University; Departments of wTraditional Chinese Medicine; and
zClinical Pharmacy, Chongqing Medical University, Chongqing,
China.
S.L. and Y.L. are corst authors.
S.L. and X.L.: participated in study design. S.L. and Y.L.: participated
in data acquisition, data analysis, and preparation of the manuscript. X.L.: gave instructions in statistical analysis. S.L., Y.L., and
X.L.: participated in data interpretation, and critical revision and
editing of the manuscript.
Supported by National Key Clinical Specialties Construction Program
of China.
Disclosure: The authors declare no conict of interest.
Reprints: Xin Liu, BS, Department of Clinical Pharmacy, Chongqing
Medical University, 1 Yi Xue Yuan Road, Yu Zhong District,
Chongqing 400016, China (e-mail: liuxin8829@sina.com).
Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
DOI: 10.1097/IJG.0000000000000357

J Glaucoma

Volume 25, Number 1, January 2016

Literature Search
A comprehensive review of the literature was conducted
by searching PubMed, Embase, the Cochrane library, the Web
of Science, and the Chinese BioMedical Literature Database
disk databases up to November 20, 2014 using a combination
of the following terms: obstructive sleep apnea or OSA
and glaucoma or open angle glaucoma or OAG or
angle closure glaucoma or ACG or normal tension
glaucoma or NTG and cohort study or case control
study with no language limitation. We also searched manually using reference lists of retrieved original articles and
recent reviews. For reliability, 2 authors (S.L. and Y.L.)
screened the searches independently. The titles and abstracts
resulting from the searches were checked, and the full text of
retrieved studies were assessed according to the inclusion and
exclusion criteria. Disagreements were resolved by reaching
consensus among all authors.

Inclusion and Exclusion Criteria

Inclusion criteria: (1) OSA was diagnosed by physicians, polysomnography or respiratory polygraphy; (2) we
only selected cohort studies or case-control studies; (3) the
relationship between OSA and risk for glaucoma in terms
of odds ratio (OR), relative risk (RR), and hazard risk
(HR) was available. Studies were excluded for the following
reasons: (1) cross-sectional study, surveys, case reports,
reviews, or meta-analysis; (2) appropriate risk estimates and
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Liu et al

J Glaucoma

Volume 25, Number 1, January 2016

95% condence intervals (CIs) not reported or could not be

computed; (3) OSA was self-reported or diagnosed by
questionnaire only; and (4) congenital glaucoma was
included.

Data Extraction and Quality Assessment

The following information were extracted: rst
authors name, publication year, number of subjects, age,
sex, study design, method used to diagnose OSA, method
for selecting participant, and inclusion, exclusion and
confounding variables. Quality assessment was based on a
widely used tool for the quality assessment of case-control
and cohort studies: the Newcastle-Ottawa Quality scale19
with a full score of nine. Studies with a score no less than 7
were considered with high quality.

Statistical Analysis
Stata 11.0 (Stata Corporation, College Station, TX)
metan command was used for the meta-analysis. A P value
of <0.05 was considered signicant. Adjusted RR/OR/HR
was extracted from the studies. As the absolute risk of
glaucoma is low, RRs and HRs are expected to yield similar
estimates of ORs. Consequently, we pooled RR, OR, and
HR together based on a random (DerSimonian-Laird) or
xed (Mantel-Haenszel) eects model depending on heterogeneity. Cochrane Q and I2 was used for the heterogeneity
test. An I2 < 50% was considered to represent a low level of
heterogeneity, 50% to 60% a moderate level, and 60% to
100% a high level. When I2 Z50%, the random-eects
model was used for pooling estimates. Otherwise, the xedeects model was used. Subgroup analysis was performed
according to glaucoma type and geographical area. Beggs
test was used for publication bias assessment. A value of
Pr > |z| <0.05 was considered to be potential publication
bias. Sensitivity analysis was conducted to evaluate the
inuence of a single study on the overall eect estimate by
stepwise omitting 1 study at a time and reevaluated the
summary eect estimates.

RESULTS
The search algorithm yielded 111 records; of them, 82
were excluded as irrelevant on the basis of title and abstract
and 4 were excluded because of duplication. The full text of
the remaining 25 studies was assessed according to the eligibility criteria, 18 studies did not meet the inclusion
criteria, leaving a total of 7 studies for this meta-analysis.12,13,15,17,18,20,21 Two cohort studies were published
from the same health database,12,13 and the study with the
largest sample size was used.12 Thus, 6 studies were analyzed (Fig. 1). The characteristics and basic information of
the included studies were presented in Tables 1 to 4. There
were 1 prospective18 and 3 retrospective cohort studies12,13,17 and 3 case-control studies.15,20,21 Several of the
included studies comprised data for >1 type of glaucoma,12,15,18 1 on both OAG and NTG,17 another 2 on
NTG.20,21 As NTG is a subgroup of OAG, we considered
these studies contained only OAG patients.17,20,21 The
selected 6 studies (Table 1) included a total of 2,288,701
people. One study were performed in Taiwan,12 2 in
USA,15,17 1 in Turkey,21 1 in France,18 and 1 in mainland of
China.20 There was only 1 case-control study with data
exclusively on males.15 All the control groups were composed of general population. Among cohort studies,
HR,12,17 OR,18 and the related CI was adjusted by confounders such as age, sex, body mass index, or other

FIGURE 1. Flow diagram showing the study selection process.

factors. Patients and controls had no statistical dierence

among confounders in case-control studies.15,20,21 ORs and
related CIs of case-control studies were calculated from the
data provided in the articles. Chen et al12 estimated HR of
both men and women, and discussed the groups under the
age of 44, between age of 45 and 54, and above the age of
55. Two studies discussed the groups in which OSA patients
received no treatment, treated with CPAP, surgery, or
multiple treatment.12,17

Quality of Included Studies

Rating of the quality of studies according to the
Newcastle-Ottawa score is presented in Table 2 and
Table 4. There quality scores ranged between 8 and 9,
therefore were considerd with high qualities.

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J Glaucoma

Volume 25, Number 1, January 2016

OSA and Glaucoma: A Meta-analysis

TABLE 1. Subjects Characteristics of Cohort Studies

Country/ Participants
References Study Design Population (% Male)
Aptel
et al18

Prospective
cohort study

France

9580 (68.0)

Chen
et al12

Retrospective
cohort study

Taiwan

Stein
et al17

Retrospective
cohort study

USA

2528 (77.8)
OSA
patients,
10,112
(77.8)
controls
156336 (59.9)
OSA
patients,
2102725
(42.1)
controls

Age Range or
Mean (y)

Follow-up Duration (y)

Confounding Variables

63.25

3y

45.1/45.1

Follow-up was ended when

the individual had
glaucoma or withdrawn
the insurance or until
December 31, 201010

Age, sex, height, weight, body

mass index, arterial
hypertension, tobacco
consumption, high cholesterol
levels, high triglyceride levels,
and thyroid dysfunction
Age, sex, hypertension, diabetes,
hyperlipidemia, and coronary
artery disease

54.2/54.8

Follow-up was ended when Age, sex, race, region of

residence within the US,
until individual had the
event (OAG, NTG) or left education level, household net
worth, diabetes mellitus,
the medical plan or
systemic arterial hypertension,
December 31, 20076
hyperlipidemia, obesity,
systemic hypotension,
migraine headache, cataract,
pseudophakia or aphakia,
diabetic retinopathy, macular
degeneration, and Charlson
Comorbidity Index (an overall
measure of health)

NTG indicates normal-tension glaucoma; OAG, open-angle glaucoma; OSA, obstructive sleep apnea.

OSA and Incidence of Glaucoma: Case-Control

Studies
A total of 3 studies including 711 cases and 6709
controls were included in meta-analysis. Under the xedeects model, the overall estimate was OR = 2.46 (95% CI,
1.32-4.59, P = 0.005) which indicates a strong association.
The test for heterogeneity produced I2 = 0.0% (Fig. 2).

OSA and Incidence of Glaucoma: Cohort Studies

Three cohort studies of 15 data sets with total sample
size of 2,281,281 were included. Under the random-eects
model, the total summary eects were OR = 1.43 (95% CI,
1.21-1.69, P = 0.000). The test for heterogeneity described
I2 = 85.5%, which indicated substantial heterogeneity
among the studies (Fig. 3).

TABLE 2. Basic Information of Cohort Studies

Inclusion
References
Aptel
et al18

Chen
et al12
Stein
et al17

OSA Assessment (Method)

PSG or respiratory polygraphy

Type of
Glaucoma

OSA Patients

Exclusion
Controls

OSA
NOS
Patients Controls Score

Not limited

AgeZ50, metabolic, cardiovascular, NA

respiratory, apnea hypopnea index
and the percentage of time at night
with oxygen saturation <90% data
available
PSG
Not limited Newly diagnosed OSA Age, sex
Diagnosed OAG
in the database from
matched
before OSA
year 2000 to 2009
with OSA
patients
82% of the OSA patients were diagnosed OAG + NTG Age > 40, beneciaries in the database NA
by pulmonologists, neurologists, sleep
who had any form of eye care from
specialists, or otolaryngologist. 60%
year 2001 to 2007
of the OSA patients had PSG or some
other formal sleep study.

NA indicates not applicable; NOS, Newcastle-Ottawa Scale; NTG, normal-tension glaucoma; OAG, open-angle glaucoma; OSA, obstructive sleep apnea;
PSG, polysomnography.

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J Glaucoma

Volume 25, Number 1, January 2016

TABLE 3. Subjects Characteristics of Case-Control Studies

Study Country/
References Design Population
Bilgin21
Dong
et al20
Girkin
et al15

Clinical
casecontrol
Clinical
casecontrol
Nested
casecontrol

Turkey
China
USA

Participants
(% Male)

Age Range or
Mean (y)

24 (37.5) NTG
patients
24 (37.5) controls
20 (70) NTG patients
18 (44.4) controls

53-78/53-77
68.1/73.2

667 (100) glaucoma

patients
6667 (100) controls

69/69

Confounding Variables
Age, sex, and systemic risk factors such as
diabetes mellitus, hypertension,
or hypercholesterolemia
Age, sex, height, weight, BMI
Ischemic heart disease, cerebrovascular, disease, lipid
metabolism disorders, hypertension, diseases of the
arteries, arterioles and capillaries, diabetes and
migraines

BMI indicates body mass index; NTG, normal-tension glaucoma.

Subgroup Analysis
There were substantial heterogeneity among the cohort
studies, therefore, geographic area (China or others) and
types of glaucoma (OAG or >1 type) were chosen as the
stratications for subgroup analyses to nd the sources of
heterogeneity. When the studies were stratied by the geographic area, heterogeneity and inconsistency among the
studies were eliminated in both subgroups (I2 = 0.0%).
Signicant positive associations were only observed in

studies conducted in China (OR = 1.86; 95% CI, 1.65-2.10,

P = 0.000) (Table 5). When the studies were divided by the
types of glaucoma, the consistency was observed among the
OAG subgroup (I2 = 0.0%) and the heterogeneity between
studies remained high for subgroup that contained >1 type
of glaucoma (I2 = 39.1%). Signicant positive association
was only observed in subgroup contained >1 type of glaucoma(OR = 1.72; 95% CI, 1.48-2.00, P = 0.000). Two
studies also reported the impact of treating OSA on

TABLE 4. Basic Information of Case-Control Studies

References

OSA
Assessment
(Method)

Inclusion
Type of
Glaucoma

Bilgin21

PSG

NTG

Dong
et al20

PSG

NTG

Girkin
et al15

Diagnosis
taken from
database,
no specic
technique
mentioned

Not
limited

Glaucoma Patients

Exclusion
Controls

(1) c/d ratio over 0.5 Age, sex, and systemic risk
or dierence of c/d
factors such as diabetes
between 2 eyes
mellitus, hypertension, or
>0.2 with thinning
hypercholesterolemia
of the neuroretinal
matched with patients
rim
(2) Glaucomatous
visual eld defects
(3) Open iridocorneal
angle
(4) IOP < 21 mm Hg
without treatment
(1) Typical changes of
NA
glaumatous
neuroretinal rim
(2) Glaucomatous
visual eld defects
(3) Open iridocorneal
angle
(4) IOP < 21 mm Hg
without treatment
AgeZ50

Glaucoma Patients

Controls

NA

(1) Severe disease of dioptric media

which interfere with the evaluation
of the fundus and visual eld
(2) Secondary glaucoma
(3) History of severe ocular trauma
(4) History of sleep disorder
(5) Medication that would inuence
sleep or on steroid
(6) Other ocular disease
(7) Systemic disease which would
inuence sleep or eye
(1) AgeZ50 and matched (1) Female (because (1) Female
with patients
female patients
(because
(2) randomly selected from
were too few in the
female
the study population who
hospital)
patients
did not have a glaucoma (2) Patients who had a were too
diagnosis by the end of
glaucoma diagnosis
few in the
the observation period
before the
hospital)
observation period
of the study (19972001)

NOS
8

c/d indicates cup/disc; IOP, intraocular pressure; NOS, Newcastle-Ottawa Scale; NTG, normal-tension glaucoma; PSG, polysomnography.

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J Glaucoma

Volume 25, Number 1, January 2016

OSA and Glaucoma: A Meta-analysis

FIGURE 2. Odds ratio (OR) for the association between obstructive sleep apnea (OSA) and glaucoma (case-control studies only).
Squares represent study-specific OR estimates (size of the square reflects the study-specific statistical weight); horizontal lines represent
95% confidence interval (CI); diamonds represent summary OR estimates with corresponding 95% CI. Figures 2 can be viewed in color
online at www.glaucomajournal.com.

glaucoma, and the pooled OR for OSA patients who got

CPAP treatment only was 1.13 (95% CI, 0.77-1.66,
P = 0.544), who got any treatment was 1.17 (95% CI, 0.891.55, P = 0.267), and those without was 1.22 (95% CI, 0.931.59, P = 0.144).

Publication Bias
Beggs test were performed to assess the publication
bias in the literature. All 6 eligible studies yielded a Beggs

test score of Pr > |z| = 0.348, which suggested that there is

no publication bias.

Sensitivity Analysis
Finally, we conducted a sensitivity analysis using
metaninf stepwise omitting 1 study at a time and reevaluated the summary ORs of remaining studies to evaluate
the inuence of a single study on the overall eect estimate.22 The results showed that no single study signicantly
inuenced the pooled ORs.

FIGURE 3. Odds ratio (OR) for the association between obstructive sleep apnea (OSA) and glaucoma (cohort studies only). Squares
represent study-specific OR estimates (size of the square reflects the study-specific statistical weight); horizontal lines represent 95%
confidence interval (CI); diamonds represent summary OR estimates with corresponding 95% CI. Figures 3 can be viewed in color
online at www.glaucomajournal.com.

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Liu et al

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Volume 25, Number 1, January 2016

TABLE 5. Subgroup Analysis of Cohort Studies

Subgroups
China
Others
Total
OAG
> 1 type
Total

No. Included Data Sets

Weight (%)

10
5
15
4
11
15

59.17
40.83
100
32.56
67.44
100

Summary OR (95% CI)

1.86
1.01
1.43
1.01
1.72
1.43

Q Test (P)

I2 (%)

0.858
0.844
0
0.888
0.088
0.000

0.0
0.0
85.5
0.0
39.1
85.5

(1.65-2.10)
(0.98-1.04)
(1.21-1.69)
(0.97-1.04)
(1.48-2.00)
(1.21-1.69)

CI indicates condence interval; OAG, open-angle glaucoma; OR, odds ratio.

DISCUSSION
This is the rst report evaluating the relationship
between OSA and glaucoma by using cohort and casecontrol studies for analysis. And the results revealed that
compared with non-OSA group, OSA group was associated
with more frequent glaucoma. Chinese OSA patients were
associated with a higher risk of developing glaucoma than
people in other countries. Higher risk may also be present
in female and younger OSA patients.
OSA is a sleep-related respiratory disturbance characterized by repeated episodes of apnea and hypopnea. It is
associated with endocrine and metabolic disturbances, such
as hypertension, metabolic syndrome, and cardiovascular
diseases.2325 The underlying etiological mechanisms for the
relationship between glaucoma and OSA remains unclear,
although there are several possible explanations. Hypoxia
and subsequent reperfusion caused by OSA will lead to
inammation.26 Furthermore, hypoxia can also increase
intracranial pressure during sleep,27 which subsequently
decrease cerebral perfusion pressure and disturb blood supply
to the optic nerve.28 Besides, increased sympathetic tone was
observed in OSA patients, which can lead to increased blood
pressure, vascular resistance, and endothelial dysfunction.29
Consequently, there may be insucient blood supplying the
retinal nerve ber layer and optic nerve.30
Because of the complexity of the relationship between
OSA and glaucoma, we only use adjusted-eect estimates in
the meta-analysis. Confounding factors such as age, sex,
endocrine and cardiovascular disease were identied in
included studies. The results from cohort studies showed
that OSA group was associated with a signicant 1.43-fold
increased risk of glaucoma, whereas case-control studies
showed a 2.46-fold increased risk. Furthermore, the results
suggested that a 72% increase in the risk was observed
when the endpoint contained >1 type of glaucoma. However, OSA did not increase the risk of OAG. In study
conducted in China, most of the patients selected were of
Han Chinese ethnicity. Chinese OSA patients were associated with a 86% relative increase in glaucoma, yet no
increased risk was observed for the patients in other
countries. This may due to the dierent incidence of glaucoma among these population. In people older than 40
years of age, the prevalence of OAG was estimated to
be 1.40% in China, 1.97% in Europe, and 1.86% in the
United States.1,31 The prevalence of ACG was estimated
to be 1.26% in China, 0.25% in Europe, 0.19% in Latin
America, and 0.16% in Africa. The incidence of glaucoma
in these countries within the same time period will be different too. The higher prevalence of OAG and lower
prevalence of ACG in other countries than that in China
may lead to the result above.

Chen et al12 showed that male OSA patients had a 75%

increase in the risk of developing glaucoma (OR = 1.75; 95%
CI, 1.30-2.35, P = 0.000), which was lower than female
patients (OR = 2.23; 95% CI, 1.37-3.64, P = 0.001). Similar
nding was observed in another study by Lin et al.13 It was
excluded from the meta-analysis because of the same database used in the study.12 They reported that HR for OAG
diagnosed among females with OSA during the 5-year follow-up period was 1.55 (95% CI, 1.04-2.31) than the control
group. However, it was only 1.45 (95% CI, 1.02-2.16) among
males. In the case-control study conducted by Girkin et al,15
no signicant relationship between OSA and glaucoma
among males was found. Younger OSA patients had greater
HR than older patients with OSA in glaucoma risk than
control.12 There was no signicant dose-response relationship
between OSA severity and glaucoma prevalence.18 Although
old age and male sex are risks for OSA or glaucoma, the
ndings above can remind the clinicians of the higher risk of
glaucoma in younger or female OSA patients. Although some
clinicians worried that CPAP would worsen glaucoma as it
would increase intraocular pressure. Our results suggested
that treatment did not increase the risk of glaucoma. However, these results were based on few studies and need to be
interpreted with caution.
The meta-analysis included both case-control and cohort
studies representing various countries, and mixes of dierent
types of glaucoma. However, certain limitations still existed.
First, the meta-analysis included 3 case-control studies, possibly, having a degree of experimental bias. Another limitation is
high heterogeneity among cohort studies. To determine the
sources of heterogeneity, subgroup analysis was conducted by
stratied geographic area and types of glaucoma. And they
were considered potential explanations of heterogeneity for the
decreasing I2 test results from these subgroups. Therefore, the
overall level of evidence found by this meta-analysis may be
reduced by these limitations.

CONCLUSIONS
On the basis of our meta-analysis of 3 case-control and
3 cohort studies, OSA was a risk factor for glaucoma,
especially in China, but may not increase the risk of OAG.
Younger and female OSA patients may be more vulnerable
than other OSA patients. Future studies should investigate
the relationship of OSA, the severity of OSA, or OSA
treatment option and glaucoma.
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J Glaucoma

Volume 25, Number 1, January 2016

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OSA and Glaucoma: A Meta-analysis

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