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CLINICAL SCIENCES
Effect of Measurement Order Between Right and Left
Eyes on Intraocular Pressure Measurement
Melike Pekmezci, MD; Sidney T. Chang, MD; Bradley S. Wilson, MA;
Mae O. Gordon, PhD; Anjali M. Bhorade, MD, MSCI
Objective: To determine whether the order of intraocular pressure (IOP) measurement between right and
left eyes affects IOP measurement.
Methods: A total of 105 healthy volunteers from the eye
clinics and staff at Washington University were randomized into 2 groups. Group 1 underwent 3 sets of 2 IOP
measurements per eye, starting with the right eye (right
eye twice, left eye twice, right eye twice). Group 2 underwent similar measurements starting with the left eye.
After 2 weeks the order of IOP measurements were reversed between groups. A mixed-model repeatedmeasures analysis of variance analyzed the association
of IOP measurement with the order measured (1) between first and second eyes, (2) between first and second visits, (3) between right and left eyes, and (4) with
ocular squeezing.
right or left eyes were measured first (P = .002). Intraocular pressure measurements decreased between the
first and second visits (P ⬍ .001). No difference was
found in IOP measurements between right and left
eyes (P = .41). Moderate and severe ocular squeezing
were associated with higher IOP measurements
(P ⬍.001) and occurred more during earlier than later
IOP measurements within a set (P ⬍ .001) and
between sets (P⬍ .001 to P=.03).
Conclusions: Intraocular pressure measured in the first
eye, whether right or left, is higher than IOP measured
in the fellow eye; this may be partially because of ocular
squeezing. Measurements of IOP decrease between first
and second visits. Multiple IOP measurements at multiple visits are necessary to accurately diagnose and treat
patients with glaucoma and ocular hypertension.
Results: Intraocular pressure measured higher in first
eyes compared with fellow eyes regardless of whether
A
Arch Ophthalmol. 2011;129(3):276-281
CCURATE INTRAOCULAR
pressure (IOP) measurements are essential for clinicians to diagnose, treat,
and manage glaucoma and
ocular hypertension. Intraocular pressure
may be affected by true physiologic processes (eg, disease, blood pressure) or artifactual influences on IOP measurement
(eg, ocular squeezing, measurement error). It is important to distinguish artifactual from physiologic effects on IOP measurement to better estimate true IOP.
Author Affiliations:
Department of Ophthalmology,
University of California,
San Francisco (Dr Pekmezci);
and the Department of
Ophthalmology and Visual
Sciences, Washington
University School of Medicine,
St Louis, Missouri (Drs Chang,
Gordon, and Bhorade and
Mr Wilson).
CME available online at
www.jamaarchivescme.com
and questions on page 266
In a recent analysis from the Ocular Hypertension Treatment Study,1 the mean (SD)
IOP of the right eye measured 0.3 (2.8)
mm Hg higher than that of the left eye. In
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276
addition, the IOP of the right eye measured higher than that of the left eye at almost every 6-month visit during a 60month period.1 Although this difference is
small, it was statistically significant, implying a true difference in IOP measurement
between right and left eyes in this study.
Other studies that measured the right eye
first also reported higher IOP measurement (0.3-0.9 mm Hg) in the right eye compared with the left.2-4 Whether this difference in IOP measurement is because of a
true physiologic difference between right
and left eyes or an artifactual difference related to the right eye being measured first
has not yet been investigated.
There are several theories for why this
small yet consistent difference in IOP
measurement between right and left eyes
exists. Patient factors such as the Valsalva maneuver and ocular squeezing are
known to elevate IOP.5-8 These factors
may be more pronounced during the
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first IOP measurement, traditionally in the right eye,
causing an erroneously higher IOP measurement in the
right eye compared with the left. In addition, ocular
dominance has been associated with higher IOP.9 If
ocular dominance affects IOP, the presence of more
right eye–dominant participants may explain the higher
IOP measurement of right eyes. To date, there are no
studies that have analyzed whether the order of IOP
measurement between right and left eyes, ocular
squeezing, or ocular dominance contribute to previously reported differences in IOP measurement between
right and left eyes.
METHODS
STUDY POPULATION
The study was approved by the institutional review board at
Washington University in St Louis, Missouri. Healthy participants aged 18 to 70 years with no major ocular disease were
recruited from ophthalmology and optometry clinics and volunteer employees at Washington University School of Medicine. All participants underwent a routine ophthalmic examination or a review of their most recent ophthalmic examination
for inclusion in the study. Patients excluded from the study were
those with a history of glaucoma or glaucoma suspect status, a
first-degree relative with glaucoma, proliferative or severe nonproliferative diabetic retinopathy, age-related macular degeneration requiring treatment, corneal pathology, severe dry eye
syndrome, uveitis, visually significant cataracts, history of cerebrovascular accident, or history of intraocular injections or intraocular or laser surgery. Demographic and clinical data of participants were recorded.
IOP MEASUREMENTS
Following informed consent, participants were randomized to
1 of 2 groups by a randomized permuted block design with equal
allocation to both groups in the study. All participants underwent 2 visits. At each visit, a set of 2 IOP measurements was
taken in the first eye, repeated in the fellow eye, and repeated
again in the first eye. At the first visit, participants in group 1
underwent IOP measurements starting with the right eye while
participants in group 2 underwent IOP measurements starting
with the left eye.
All attempts were made to schedule the second visit within
2 weeks of the first and within 2 hours of the time of day as the
first visit to reduce effects of diurnal variation on IOP. At the
second visit, participants underwent the same sets of IOP measurements as the first visit but starting with the opposite eye.
All IOP measurements were conducted in a similar manner for both visits. One drop of a combined solution of fluorescein sodium, 0.25%, and benoxinate hydrochloride, 0.4%,
was instilled in both eyes prior to the first set of IOP measurements. The drop was instilled in each eye in the same sequence as the order of the IOP measurement (eg, if the right
eye was measured first, the fluorescein was applied to the right
eye first). If the participant wore contact lenses, they were asked
to remove them 10 to 15 minutes prior to the IOP measurements. All IOP measurements were performed using a calibrated Goldmann applanation tonometer, with one examiner
measuring the IOP and rotating the tonometer dial and a second examiner reading and recording the IOP measurement from
the tonometer dial. The tonometer dial was rotated to 10 mm Hg
prior to all measurements. All measurements were performed
by a single examiner (M.P.) who was right-handed, while all
IOP readings were performed by 1 of 3 examiners. Participants were reminded to breathe naturally and maintain fixation at a distance before each measurement. After all IOP measurements were obtained, the central corneal thickness of each
eye was measured using a System Corneo-Gauge III ultrasound pachymeter (Chiron IntraOptics Inc, Irvine, California) with the lowest of 3 consecutive measurements recorded
as the central corneal thickness for each eye.
OCULAR SQUEEZING
The degree of ocular squeezing during each IOP measurement
was graded by the same examiner who measured IOP (M.P.)
using the following scale: none, IOP measured on the first attempt with no difficulty and no ocular squeezing; mild, IOP
measured on the first attempt with no difficulty but mild ocular squeezing; moderate, IOP measured on the first or second
attempt with some difficulty due to ocular squeezing; severe,
IOP measured on the second or third attempt with great difficulty due to ocular squeezing; and unable, unable to measure
IOP because of extreme ocular squeezing and/or discomfort reported by the participant.
OCULAR DOMINANCE TESTS
The pointing-a-finger, hole-in-card, and hole-in-card at face tests
were performed to determine the dominant eye of each participant.10,11 The overall dominant eye was the eye deemed dominant by at least 2 of the 3 ocular dominance tests. If the tests
were inconclusive then the dominant status was recorded as
undetermined.
STATISTICAL ANALYSIS
Descriptive statistics (means and standard deviations) are reported for all IOP measurements obtained at both visits and
the proportion of moderate or severe ocular squeezing recorded during IOP measurements by each set, within a set, and
by each visit. Mixed-models, repeated-measures analysis of variance (Proc Mixed in SAS version 9.2; SAS Inc, Cary, North Carolina) were designed to test for differences in IOP measurement between: (1) sets of IOP measurements (first set vs second
set vs third set), (2) IOP measurements within each set (first
IOP measurement vs second IOP measurement), (3) first and
second visits, (4) right and left eyes, (5) no or mild vs moderate or severe ocular squeezing, and (6) dominant vs nondominant eyes. Generalized estimating equations for repeated categorical data (Proc Genmod; SAS Inc) were designed to test for
differences in moderate or severe ocular squeezing due to the
order it was measured between (1) sets of IOP measurements,
(2) IOP measurements within each set, and (3) first and second visits. Because of the relatively low incidence of ocular
squeezing, the effects of ocular laterality and dominance were
not included in this model.
RESULTS
Between January 2, 2008, and June 30, 2008, 148 of 194
screened patients met eligibility criteria for the study. Of
the eligible participants, 108 agreed to participate in the
study; however, 3 were later excluded because of difficulty measuring IOP (2 participants) and erratic IOP measurements (1 participant). Of the 105 participants included in the analysis, 50 (48%) were randomized to group
1 and 55 (52%) to group 2.
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Table 1. Participant Characteristics
Visit 1
Visit 2
15.5
No. (%)
Sex
Male
Female
Age, mean (SD), y
Race
White
African American
Asian
Hispanic
Recruitment site
Eye clinic
Volunteer staff
Contact lens wearer
Yes
No
Ocular diagnosis
Mild cataracts
Mild dry eyes
Other
Ocular medications
None
Artificial tears
Ketorolac
Distance spherical equivalent,
mean (SD), diopter
Right eye
Left eye
Central corneal thickness,
mean (SD), µm
Patients, No.
Right eye
Left eye
a ␹2 Test.
b Independent
21 (42)
29 (58)
40.3 (13.2)
Group 2
(n=55)
20 (36)
35 (64)
38.8 (12.4)
IOP, mm Hg
Group 1
(n=50)
Characteristic
15.0
P
Value
.55 a
14.5
14.0
Group 1, right eye
Group 1, left eye
Group 2, right eye
Group 2, left eye
13.5
13.0
12.5
.55 b
1
2
3
4
5
6
7
8
9
10
11 12
Measurement Order
36 (72)
9 (18)
4 (8)
1 (2)
39 (71)
9 (16)
5 (9)
2 (4)
.95 a
38 (76)
12 (24)
42 (76)
13 (24)
.97 a
11 (22)
39 (78)
13 (23)
43 (77)
.84 a
7 (14)
6 (12)
6 (12)
2 (4)
10 (18)
6 (11)
.058 a
.38 a
.86 a
47 (94)
3 (6)
0 (0)
51 (93)
3 (5)
1 (2)
.63 a
−2.2 (2.4)
−2.1 (2.6)
−1.7 (2.9)
−1.7 (2.9)
.36 b
.41 b
49
559.3 (33.6)
557.1 (32.2)
55
557.0 (36.9)
558.9 (37.7)
.74 b
.81 b
Figure 1. Intraocular pressure (IOP) measurements by measurement order
and visit order for groups 1 and 2.
t test.
There were no statistically significant differences in
baseline characteristics between the 2 groups (Table 1).
Both visits were completed for 47 participants (94%) in
group 1 and 48 (87%) in group 2. The second visits occurred within 2 weeks of the first visit in 42 participants
(89%) in group 1 and 34 (71%) in group 2. Furthermore, the second visits were scheduled within 2 hours
of the first visit in 36 participants (77%) in group 1 and
37 (77%) in group 2.
RELATIONSHIP OF IOP
TO MEASUREMENT ORDER
All 12 IOP measurements (means [standard deviations]) obtained for each group on both visits are displayed in Figure 1. There was no overall difference in
IOP measurement between the 2 groups (P = .41); thus,
the following results reflect the combined IOP measurements from both groups.
At both visits, the initial IOP measurement obtained
in each eye was higher in the first eye than in the second. For example, when the right eye was measured first,
its initial IOP measurement (mean [SD], 15.1 [2.6]
mm Hg) was higher than the initial IOP measurement
of the left eye (14.1[2.3] mm Hg) and when the left eye
was measured first, its initial IOP measurement (14.8[2.2]
mm Hg) was higher than the initial IOP measurement
of the right eye (14.2[2.0] mm Hg). Regardless of which
eye was measured first, there was a significant difference in IOP measurement between the first and second
eyes (first set vs second set P =.002). There was also a
significant decrease in IOP measurement between the first
and second measurements within a set (obtained from
the same eye) and between the first and second visits
(Table 2).
There was no statistically significant difference in mean
IOP measurements obtained from both visits between right
and left eyes (P =.41).
RELATIONSHIP OF IOP
TO OCULAR SQUEEZING
There was no statistically significant difference in moderate or severe ocular squeezing between group 1 (mean
8.5%) and group 2 (mean, 4.0%) for all IOP measurements obtained at both visits (P=.17). Therefore, the results for ocular squeezing reflect the combined results
from groups 1 and 2.
Moderate or severe ocular squeezing occurred in 75
of 1200 measurements obtained (6.3%) and was associated with higher IOPs compared with measurements
with no or mild ocular squeezing (Table 2). There was
a significant decrease in moderate or severe ocular
squeezing between the first and second IOP measurements within a set, the first and second sets, and the
second and third sets (Figure 2). No significant difference in moderate or severe ocular squeezing was
found between the first and second visits or right and
left eyes.
RELATIONSHIP OF IOP
TO OCULAR DOMINANCE
The overall dominant eye was the right eye in 55 participants (52.4%), the left eye in 46 participants
(43.8%), and undetermined in 4 participants
(3.8%). There was no significant difference in IOP
(P = .39) between dominant and nondominant eyes
(Table 2).
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IOP,
Mean (SD),
mm Hg
Subclassification
IOP by set
First set (n = 400)
Second set (n =400)
Third set (n = 400)
IOP within a set
First measurement
(n = 600)
Second measurement
(n = 600)
IOP by visit
First visit (n = 630)
Second visit (n =570)
IOP by eye
Right eye (n = 596)
Left eye (n = 604)
IOP by ocular squeezing
None/mild (n = 1125)
Moderate/severe (n=75)
IOP by ocular dominance
Nondominant eye (n=582)
Dominant eye (n=582)
Eyes With Moderate/Severe Ocular Squeezing, %
Table 2. Intraocular Pressure Measurements
by Subclassification for All Participants
Value a
P
14.5 (2.3)
14.2 (2.3)
14.2 (2.3)
.002 (First vs second set)
.48 (Second vs third set)
.0002 (First vs third set)
14.4 (2.3)
⬍.001
14.2 (2.3)
11.0
10.0
9.0
8.0
7.0
6.0
5.0
4.0
3.0
2.0
1.0
0.0
First Second
14.7 (2.4)
13.9 (2.1)
.001
14.3 (2.3)
14.2 (2.3)
.41
14.2 (2.3)
14.9 (2.4)
.001
14.3 (2.4)
14.2 (2.2)
.39
Abbreviation: IOP, intraocular pressure.
a Mixed-model, repeated-measures analysis of variance.
COMMENT
To our knowledge, this is the first study that investigates whether the order of IOP measurement between
right and left eyes plays a role in previously reported IOP
asymmetry between right and left eyes.1-4 We found that
the IOP measured in the first eye, whether the right or
left, was higher than the IOP measured in the fellow eye.
Thus, prior reports of higher IOP measurements in right
than left eyes are likely because of the right eyes being
measured first and not a physiologic difference in IOP
between eyes.
We also report a decrease in IOP measurements with
repeated applanation tonometry both within a visit and
between 2 visits. Previous studies demonstrated this same
phenomenon and at values comparable with our 0.3–mm
Hg decrease in IOP measurement in the same eye (ie, between the first and third sets of IOP measurements).12-14
Other studies, however, did not specifically test whether
the order of IOP measurement between right and left eyes
explains the asymmetry between IOP measurement of
right and left eyes.
Why is IOP measured higher in initial as opposed to
fellow eyes and why does IOP decrease with repeated applanation tonometry? One plausible explanation is that
patients have more anxiety and unfamiliarity with tonometry during earlier IOP measurements, causing artifactually higher IOPs than those measured later. Patients who receive sham tonometry prior to real tonometry
measured IOP 2 mm Hg lower than patients without sham
tonometry, suggesting that familiarity with applanation
tonometry may result in a lower measured IOP.13 Ocular squeezing, Valsalva maneuver, or other unknown phe-
1
Measurement
Within a Set∗
2
3
Set∗
1
2
Visit
Right
Left
Eye
Figure 2. Percentage of eyes with moderate/severe ocular squeezing during
intraocular pressure measurements. *P ⬍ .001.
nomena associated with anxiety or unfamiliarity with tonometry may play a role in the higher initial IOP
measurements.
Attempted eyelid closure, or ocular squeezing, has
been associated with increased IOP measurement by
Goldmann applanation tonometry in patients without
glaucoma 15 (1.5 mm Hg) and those with normaltension (3.9 mm Hg) and high-tension (4.1 mm Hg)
glaucoma.16 Our study confirms that IOP measurements associated with moderate or severe ocular
squeezing are higher than IOP measurements associated with no or mild ocular squeezing. Furthermore,
we found that moderate or severe ocular squeezing
occurred more frequently during earlier IOP measurements and decreased with repeated tonometry at each
visit. These results suggest that decreased IOP measurement with repeated tonometry may be partially
related to decreased ocular squeezing with repeated
tonometry. In addition, it is well known that IOP
increases with activities related to breath-holding (eg,
Valsalva) and eccentric or upward gazing.5,17-19 While
our participants were reminded to breathe naturally
and maintain fixation at distance, it is possible that
participants with anxiety or unfamiliarity with tonometry may exhibit more of these behaviors with earlier
IOP measurements.
Another factor that may explain why IOP measurement decreases with repeated applanation tonometry is
the changing status of the tear film, with a smaller tear
meniscus associated with IOP underestimation.20,21 Previous studies performing tonography in one eye report
a decrease in IOP measurement in the fellow eye, likely
because of evaporation of the tear film.22 Evaporation of
the tear film over time may occur naturally or because
of increased contact time with a topical anesthetic.13 In
addition, prolonged contact of the topical anesthetic with
fluorescein may cause fluorescein “quenching,” resulting in hypofluorescence and an underestimation of IOP
measurement.21,23 Therefore, both increased tear film
evaporation and fluorescein quenching have a greater
effect over time and may be related to the decrease in IOP
measurement with repeated applanation tonometry.
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An interesting finding in our study was the 0.8–mm Hg
mean decrease in IOP measurement between the first and
second visits. This decrease is comparable with the 0.6–
mm Hg mean decrease in IOP measurement reported between the baseline and first follow-up visit in untreated participants in the Ocular Hypertension Treatment Study.1
These differences are likely not due to evaporation of the
corneal tear film or fluorescein quenching, and we did not
find a significant difference in ocular squeezing between
visits. Effects of diurnal variation or changes in ocular or
physical health affecting IOP measurements are unlikely
in our study given that most visits were scheduled within
2 weeks and within 2 hours of the same time of day. Other
factors affecting tonometry not examined in our study (eg,
Valsalva, eccentric gaze) may differ between visits resulting in the lower IOP measurements at the second visit.
In a study by Dane et al,9 right eye–dominant patients had a mean IOP that was 0.76 mm Hg higher in
right than left eyes. Because dominant eyes perform most
of the near work, the greater accommodative effort required in dominant eyes may result in a higher IOP. We
analyzed whether ocular dominance may account for
higher IOPs in right than left eyes but we did not find a
significant difference in IOP measurement between dominant and nondominant eyes.
The results of this study emphasize that the order
of IOP measurement between right and left eyes may
affect IOP measurement, with the first eye measuring
higher than the second eye. In addition, IOP measured
on the first visit may be higher than IOP measured on
the second visit. Therefore, a single IOP measurement
taken on a single visit may not reflect the true IOP of
that eye. Artifactual influences may cause earlier IOP
measurements to appear higher (eg, more squeezing
on earlier measurements) or later IOP measurements
to appear lower (eg, evaporation of corneal tear film
over time) than true IOP. Such information is important since many clinicians establish a baseline or target
IOP or assess medication efficacy based on a single
IOP measurement at a single visit. During a medication trial, a decrease in IOP at a second visit may be
interpreted as a successful medication trial as opposed
to normal regression to the mean. Because of the multiple known and unknown factors that affect IOP measurement, we recommend multiple IOP measurements
be recorded at each visit. Factors that affect IOP measurement such as the amount of ocular squeezing
should be routinely recorded to alert for possible inaccurate measurements. In addition, baseline and target
IOPs as well as medication assessment should be
evaluated over multiple visits.
The mean differences in IOP measurements in our
study were small but may have clinical significance. Results from the Early Manifest Glaucoma Trial suggest that
even a 1–mm Hg increase in IOP was associated with an
11% increase in the hazard ratio for the progression of
glaucoma.24 Thus, measuring IOP accurately is critical
in the management of glaucoma. The values we report
are mean values, with some patients having larger differences between IOP measurements that may be clinically significant. In addition, our study analyzed the effect
of measurement order on IOP of participants with healthy
eyes; this effect may be even greater in patients with
glaucoma.
The strengths of this study include the randomization scheme with repeated measures, crossover design,
and standardized method of IOP measurement using a
2-operator system to minimize measurement bias. The
use of 1 examiner to measure IOP reduced the effect of
varying technique but may have introduced a bias (eg,
handedness) that affected the IOP measurements. Future studies may use several masked examiners to further reduce the potential bias and possibly reflect a more
clinical setting. In addition, the assessment of ocular
squeezing in our study was subjective. Our results imply that IOP measurement decreases with repeated applanation tonometry within a visit and between 2 visits;
however, factors affecting this phenomenon need to be
further elucidated.
In conclusion, we found that IOP measured in the
first eye, whether the right or left, was higher than IOP
measured in the fellow eye and IOP measurement in
both eyes decreased with repeated applanation tonometry. Clinicians should be aware of this phenomenon
and obtain multiple IOP measurements on multiple
visits to establish accurate baseline and treated IOPs to
determine medication efficacy in patients with
glaucoma.
Submitted for Publication: March 9, 2010; final revision received June 3, 2010; accepted June 16, 2010.
Correspondence: Anjali M. Bhorade, MD, MSCI, Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, 660 S Euclid Ave,
Campus Box 8096, St Louis, MO 63110 (bhorade@vision
.wustl.edu).
Author Contributions: Dr Bhorade had full access to
all of the data in the study and takes responsibility for
the integrity of the data and the accuracy of the data
analysis.
Financial Disclosure: None reported.
Additional Contributions: The authors thank Michael
Lachtrup, OD, Jamie Kambarian, and Renee Bulla for their
assistance with recruiting participants and reading IOP
measurements for this study.
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