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RESEARCH ARTICLE
Intraocular Pressure Rise in Subjects with and
without Glaucoma during Four Common
Yoga Positions
Jessica V. Jasien
1
*, Jost B. Jonas
2
, C. Gustavo de Moraes
3
, Robert Ritch
1
1 Einhorn Clinical Research Center, New York Ear Eye and Ear Infirmary of Mount Sinai, New York, New
York, United States of America, 2 Department of Ophthalmology, Medical Faculty Mannheim of the
Ruprecht-Karls-University of Heidelberg, Seegartenklinik Heidelberg, Germany, 3 Department of
Ophthalmology, Columbia University Medical Center, New York, New York, United States of America
* jjasien.ganyresearch@gmail.com
Abstract
Purpose
To measure changes in intraocular pressure (IOP) in association with yoga exercises with a
head-down position.
Methods
The single Center, prospective, observational study included 10 subjects with primary
open-angle glaucoma and 10 normal individuals, who performed the yoga exercises of
Adho Mukha Svanasana, Uttanasana, Halasana and Viparita Karani for two minutes each.
IOP was measured by pneumatonometry at baseline and during and after the exercises.
Results
All yoga poses were associated with a significant (P<0.01) rise in IOP within one minute
after assuming the yoga position. The highest IOP increase (P<0.01 ) was measured in the
Adho Mukha Svanasana position (IOP increase from 17±3.2 mmHg to 28±3.8 mmHg in
glaucoma patients; from 17±2.8 mmHg to 29±3.9 mmHg in normal individuals), followed by
the Uttanasana position (17±3.9 mmHg to 27±3.4 mmHg (glaucoma patients) and from 18
±2.5 mmHg to 26±3.6 mmHg normal individuals)), the Halasana position (18±2.8 mmHg to
24±3.5 mmHg (glaucoma patients); 18±2.7 mmHg to 22±3.4 mmHg (normal individuals)),
and finally the Viparita Kirani position (17±4 mmHg to 21±3.6 mmHg (glaucoma patients);
17±2.8 to 21±2.4 mmHg (normal individuals)). IOP dropped back to baseline values within
two minutes after returning to a sitting position. Overall, IOP rise was not signific antly differ-
ent between glaucoma and normal subjects (P = 0.813), all though glaucoma eyes tended
to have measurements 2 mm Hg higher on average.
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 1/16
OPEN ACCESS
Citation: Jasien JV, Jonas JB, de Moraes CG, Ritch
R (2015) Intraocular Pressure Rise in Subjects with
and without Glaucoma during Four Common Yoga
Positions. PLoS ONE 10(12): e0144505. doi:10.1371/
journal.pone.0144505
Editor: Haotian Lin, Sun Yat-sen University, CHINA
Received: March 26, 2015
Accepted: November 18, 2015
Published: December 23, 2015
Copyright: © 2015 Jasien et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information files.
Funding: Supported by donations from Joseph M.
Cohen to the New York Glaucoma Research Institute,
New York, NY and New York Glaucoma Research
Institute, New York, NY.
Competing Interests: The authors have declared
that no competing interests exist.
Conclusions
Yoga exercises with head-down positions were associated with a rapid rise in IOP in glau-
coma and healthy eye s. IOP returned to baseline values within 2 minutes. Future studies
are warranted addressing whether yoga exercise associated IOP changes are associated
with simi lar changes in cerebrospinal fluid pressure and whether they increase the risk of
glaucoma progression.
Trial Registration
ClinicalTrials.gov #NCT01915680
Introduction
Glaucoma is the leading cause of irreversible blindness in the United States and can dramati-
cally affect the quality of life for patients with moderate to severe visual loss. Primary open
angle glaucoma is a progressive, chronic optic neuropathy characterized by a specific pattern of
optic disc and visual field loss secondary to death of retinal ganglion calls and their axons and
represents the final common pathway of multiple diseases which affect the eye. Elevated intra-
ocular pressure (IOP) is the most common known risk factor for glaucomatous damage and, at
the current time, the only modifiable one for which treatment has a proven effect on preventing
or slowing the progress of the disease.
IOP increases on assuming a body position other than seated or upright. [1–7] A small vari-
ation can be detected when moving from the sitting to the recumbent position.[7–10] The
increase in IOP is directly related to the inclination of the body toward the completely inverted
position.[11, 12] IOP begins to rise upon assuming a head down position and with the body
vertical, which results in doubling of the IOP[13], and IOP remains elevated as this position is
maintained.[14–16] The extent of IOP fluctuations are correlated with the change of position
based on angle (ninety degrees upright or inverted) and the length of time maintained. [5, 6,
11, 13, 15].
A relationship between posture-induced IOP fluctuations and visual field loss in glaucoma
patients has been observed. Hirooka and Shiraga[5] reported that the greatest IOP fluctuation
occurred in eyes with more severe glaucomatous optic nerve damage. The extent of increased
IOP as measured in the horizontal supine position was associated with visual field damage in
normal tension glaucoma in the horizontal position.[17]
Yoga has become a popular practice in the western world, and by 1998, an estimated 15 mil-
lion American adults had performed yoga at least once. [16, 18–20] Elevation of IOP occurs
during and following the sirsasana (head stand) posture, particularly in glaucoma patients.[16,
18, 20, 21] There was a uniform 2-fold increase in IOP in this position. [16, 20– 22]
Methods
This was a prospective, observational study with a cohort of twenty subjects tested at the Ein-
horn Clinical Research Center, New York Eye and Ear Infirmary, New York, NY. The study
was approved by the New York Eye and Ear Infirmary Institutional Review Board on March
12, 2013 and conformed to the tenets of the Declaration of Helsinki and approved under clini-
cal trials registration identifier NCT01915680 on July 12, 2013. Written informed consent was
obtained from all individuals. Participant recruitment started in June 2013 and was completed
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 2/16
in September 2013; this time frame includes all study participant visits. The authors confirm
that all ongoing and related trials for this study are registered. The delay in approval of clinical
trial registration was due to study approval on clinicaltrials.gov. The CONSORT flow diagram
is shown in Fig 1.
Each participant assumed the four common yoga poses of Adho Mukha Svanasana, Uttana-
sana, Halasana and Viparita Karani in this respective order (Fig 2) within one hour. We mea-
sured the IOP of both eyes of the subjects prior to each pose in a seated position, immediately
at the start of the pose, 2 minut es into the pose, immediately after assuming a seated position,
and 10 minut es later in a seated position. IOP was measured using a Reichert Model 30 pneu-
matonometer, which was tested and calibrated using the calibration verifier before measuring
each individual. Tetracaine was administered to each eye prior to IOP measurement using the
calibrated pneumatonometer.
Fig 1. CONSORT Flow Diagram.
doi:10.1371/journal.pone.0144505.g001
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 3/16
The Adho Mukha Svanasana pose, most commonly known as “downward facing dog”, was
the first pose held by all subjects. Uttanasana, most commonly known as the “standard forward
bend pose”, was then performed. The third position performed was Halasana, most commonly
known as “plow pose” . Lastly, Viparita Karani, most commonly known as “legs up the wall
pose” was performed to complete the sequence (Fig 2).[23]
The diagnosis of bilateral primar y open-angle glaucoma was based on the presence of glau-
comatous optic nerve head changes and visual field loss, gonioscopically open anterior cham-
ber angles and no identifiable secondary cause of glaucoma. Optic nerve head changes as
assessed on stereoscopic photographs included focal or diffuse thinning of the neuroretinal
rim, focal or diffuse loss of the retinal nerve fiber layer, or an inter-eye difference in the vertical
cup-to-disc diameter ratio of >0.2 not explained by inter-eye differences in optic disc size. Cri-
teria for glaucomatous visual field loss, tested by the 24–2 Swedish Interactive Thresholding
Algorithm (SITA) (SITA-SAP, Humphrey Visual Field Analyzer; Carl Zeiss Meditec, Inc.,
Dublin, CA) were a glaucoma hemifield test result outside normal limits on at least two conse-
cutive reliable examinations or the presence of at least three contiguous test points on the pat-
tern standard deviation plot with P <1%, and with at least one of P <0.5%, not including
points at the edge of the field or those directly above and below the blind spot. All 24–2 visual
fields had to have reliability indices of <25% for fixation losses, false-positive responses and
false-negative responses.
Statistical analysis was carried out with commercially available software (STATA, version
12; StataCorp LP, College Station, TX). All continuous variables, except visual field mean
deviation (MD), followed a Gaussian distribution based on visual inspection of Q-Q plots and
the Shapiro-W test (all P > 0.10). Ther efore, all descriptive statistics are presented with
mean ± standard deviation unless otherwise specified. To explore adequacy of a linear model
when testing the relationship between IOP and the set of predictors, we plotted the histograms
of residuals and the relationshi p between fitted values and residuals to test for homoscedastic-
ity. IOP changes for each subject and each yoga position were tested with the mixed-effects lin-
ear models (MELM). Multilevel MELM anal ysis was performed at three levels: 1) position type;
2) diagnostic groups (glaucoma vs. healthy); and 3) each subject at different time points.
For the multilevel MELM results interpretation, the interaction term ‘Pose
Time’ provides a
test for differential IOP over time due to the different poses investigated; the interaction term
‘Group
Pose’ provides a test for differences in average IOP across poses due to diagnostic
groups (i.e.: glaucoma vs normal); and the interaction term ‘Group
Time
Pose’ provides a test
for differential IOP over time for each pose due to diagnostic groups.
The model was fitted with fixed coefficients (fixed effect) of participants baseline age
(years), time (prior to each pose in a seated position, immediately at the start of the pose, 2
minutes into the pose, immediately after assuming a seated position, and 10 minutes later in a
Fig 2. Scheme Illustrating the Various Yoga Positions.
doi:10.1371/journal.pone.0144505.g002
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 4/16
seated position), BMI (kg/m
2
), diagnostic group (glaucoma or control), and Yoga pose. The
random coefficient (random effect) relates to the subject (i.e.: each eye nested within subject)
to detect the effect of posture changes over time. The inclusion of random eye effects accounts
for the non-independence of the 2 eyes from the same subject. The covariance structure at each
level was treated as compound symmetric (exchangeable). Glaucoma diagnosis, body mass
index, and age were entered as predictors. Since the categorical predictor ‘Diagnostic group
(glaucoma vs. normal) is highly correlated with the variable ‘MD’, we chose to remove the vari-
able ‘MD’ from the analysis of predictors associated with IOP change. After fitting the MELM,
we plotted histograms of the residuals to evaluate whether the residuals are consistent with
normally distributed errors (Fig 3).
Finally, we performed an anal ysis of contrasts with baseline IOP values for each yoga pose
against each other to check against ‘carry-over’ (or sequence) effects, that is, whether the fact
that subjects did not assume the poses in random order could have affected our results. In addi-
tion, this analysis provides estimates and contrasts versus baseline for each yoga pose. The
same type of analysis was performed for estimates and contrasts involving comparisons among
poses, diagnostic groups, and time. Statistical significance was declared at the 0.05 level.
Results
The study included 10 subjects (9 women; median age: 62 years ± 15.5 years) with primary
open-angle glaucoma and 10 healthy individuals (8 women; median age: 36 years ± 12.4 years)
(Table 1). The difference in age between both groups was statistically significant (P<0.001).
The median of the mean visual field defect of the glaucoma patients was -9.49 dB (interquartile
rage: -1.67 dB to -21.13 dB). Regressions diagnostics of the MELM are shown in Fig 2. The
Fig 3. Histogram and test for homoscedasticity of the mixed effects linear model.
doi:10.1371/journal.pone.0144505.g003
Table 1. Demographic and Baseline Characteristics of Study Participants.
Characteristic Primary Open-Angle Glaucoma Participants Healthy Participants
Number of Participants 10 10
Females (%) 90 80
Mean age in years 62 ± 15.5 36 ± 12.4
Mean BMI in kg (m
2
) 22.1 23.8
doi:10.1371/journal.pone.0144505.t001
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 5/16
normal distribution of the residuals and the spread of the residuals relative to fitted values
(homoscedasticity) suggest adequacy of the model, the results of which are described below.
Within both groups, IOP increased significantly for all 4 yoga positions (repeated-measures
ANOVA; all P<0.001). The Adho Mukha Svanasana position was associated with the highest
IOP increase ( P<0.01) (Fig 4 ). IOP increased from 16.7 ± 3.0 mmHg (median: 17 mmHg;
range: 12, 23) to 28.5 ± 3.8 mmHg (median: 28 mmHg; range: 19, 38) at two minutes of holding
the pose. The maximum increase in IOP, measured immediately after taking the pose or at two
minutes of holding the pose, did not differ significantly (P = 0.57) between the control group
(12.6 ± 3.5 mmHg; median: 12 mmHg; range: 8 mmHg, 19 mmHg) and the glaucoma group
(11.6 ± 3.2 mmHg; median: 10 mmHg; range: 6 mmHg, 17 mmHg) (Table 2). Related to the
baseline values, the IOP increased by 79 ± 31% (median: 75%; range: 38%, 158%) in the control
group and by 72 ± 29% (median: 61%; range: 40%, 126%) in the glaucoma group. All eyes
showed an increase in IOP during the pose.
During the Uttanasana pose, IOP increased from 17.7 ± 3.1 mmHg (median: 18 mmHg;
range: 12, 25) to 26.2 ± 3.3 mmHg (median: 27 mmHg; range: 19, 33) at two minutes of holding
the pose (Fig 5). The maximum increase in IOP, measured immediately after taking the pose or
at two minutes of holding the pose, did not differ significantly (P = 0.16) between the control
group (8.4 ± 3.4 mmHg; median: 9 mmHg; range: 2 mmHg, 15 mmHg) and the glaucoma
group (9.8 ± 2.7 mmHg; median: 9 mmHg; range: 6 mmHg, 15 mmHg) (Table 2 ). Relate d to
the baseline values, the IOP increased by 48 ± 21% (median: 49%; range: 7%, 86%) in the con-
trol group and by 61 ± 26% (median: 48%; range: 24%, 107%) in the glaucoma group. All eyes
showed an increase in IOP during the pose.
Fig 4. Least squares means and mean values of the covariates of the changes in IOP in the Adho
Mukha Svanasana position over time. The X axis represents each time point an IOP measurement was
taken (0 = Baseline seated; 1 = Immediate position; 2 = 2 minutes position; 3 = Post position seated; and
4 = 10 minutes post position seated). The Y axis represents the IOP in mmHg after adjusting for the
covariates. Subjects with glaucoma diagnosis are depicted ‘Glaucoma = 1’; controls are ‘Glaucoma = 0’.
doi:10.1371/journal.pone.0144505.g004
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 6/16
During the Halasana position, IOP increased from 18.0 ± 2.6 mmHg (median: 18 mmHg;
range: 13, 23) to 22.5 ± 3.5 mmHg (median: 22 mmHg; range: 14, 31) at two minutes of holding
the pose (Fig 6). The maximum increase in IOP, measured immediately after taking the pose or
at two minutes of holding the pose, did not differ significantly (P = 0.29) between the control
group (4.7 ± 3.1 mmHg; median: 5 mmHg; range: -2 mmHg, 10 mmHg) and the glaucoma
group (5.7 ± 2.6 mmHg; median: 6 mmHg; range: 0 mmHg, 10 mmHg) (Table 2 ). Relate d to
the baseline values, the IOP increased by 28 ± 19% (median: 31%; range: -8%, 54%) in the con-
trol group and by 33 ± 17% (median: 35%; range: 0%, 67%) in the glaucoma group. All but one
eye in the control group showed an increase in IOP during the pose.
During the Viparita Kirani position, IOP increased from 17.4 ± 3.3 mmHg (median: 17
mmHg; range: 12, 26) to 20.2 ± 3.1 mmHg (median: 20 mmHg; range: 13, 27) at two minutes
of holding the pose (Fig 7). The maximum increase in IOP, measured immediately after taking
the pose or at two minutes of holding the pose, did not differ significantly (P = 0.65) between
the control group (4.0 ± 2.2 mmHg; median: 4 mmHg; range: 1 mmHg, 9 mmHg) and the glau-
coma group (3.7 ± 1.5 mmHg; median: 3 mmHg; range: 1 mmHg, 6 mmHg) (Table 2). Related
Table 2. Interquartile Range, Mean and Standard Deviations (SD) of Intraocular Pressure in Normal Individuals and Glaucoma patients for Each
Yoga Position and Time Point.
Baseline
Seated
Immediate
Position
Two Minutes
Position
Post Position
Seated
Ten Minutes Post
Position Seated
Maximal Difference
in Intraocular
Pressure between
Baseline and
Holding the Pose
Adho Mukha Svanasana mmHg %
Normals Mean ± SD 16.6 ± 2.8 28.1 ± 4.2 28.8 ± 3.9 17.9 ± 2.6 19.0 ± 2.5 12.6 ± 3.5 79 ± 31%
Glaucoma Mean ± SD 16.9 ± 3.2 27.3 ± 4.3 28.1 ± 3.8 17.6 ± 3.7 17.3 ± 3.8 11.6 ± 3.2 72 ± 29%
Normals 25%, 50%,
75%
14, 17, 18 25, 27, 32 27, 28, 32 17, 18, 20 17, 18, 20
Glaucoma 25%, 50%,
75%
14, 17, 19 26, 28, 30 27, 28, 31 15, 19, 20 15, 18, 20
Uttanasana
Normals Mean ± SD 18.0 ± 2.5 25.3 ± 3.8 26.1 ± 3.6 18.1 ± 3.1 18.3 ± 3.0 8.4 ± 3.4 48 ± 21%
Glaucoma Mean ± SD 17.3 ± 3.8 26.6 ± 3.2 26.5 ± 3.0 18.1 ± 4.4 17.5 ± 3.3 9.8 ± 2.7 61 ± 26%
Normals 25%, 50%,
75%
17, 18, 20 22, 26, 29 23, 26, 28 17, 18, 20 16, 18, 20
Glaucoma 25%, 50%,
75%
15, 18, 20 26, 27, 29 26, 27, 28 14, 19, 21 15, 18, 20
Halasana
Normals Mean ± SD 17.8 ± 2.7 21.5 ± 2.7 21.9 ± 3.4 16.8 ± 2.0 16.5 ± 2.0 4.7 ± 3.1 28 ± 19%
Glaucoma Mean ± SD 18.2 ± 2.6 23.1 ± 2.6 23.1 ± 3.6 18.4 ± 2.9 18.1 ± 3.5 5.7 ± 2.6 33 ± 17%
Normals 25%, 50%,
75%
16, 18, 20 20, 22, 23 20, 22, 24 16, 17, 18 15, 16, 18
Glaucoma 25%, 50%,
75%
16, 19, 20 21, 23, 25 21, 22, 24 17, 18, 20 16, 18, 21
Viparita Karani
Normals Mean ± SD 17.2 ± 2.8 20.7 ± 2.4 20.1 ± 2.6 17.0 ± 3.2 16.6 ± 2.2 4.0 ± 2.2 25 ± 16%
Glaucoma Mean ± SD 17.6 ± 3.8 21.0 ± 3.4 20.4 ± 3.5 17.8 ± 3.2 17.2 ± 3.2 3.7 ± 1.5 23 ± 12%
Normals 25%, 50%,
75%
16, 17, 19 19, 21, 22 18, 20, 22 15, 16, 18 15, 16, 18
Glaucoma 25%, 50%,
75%
15, 18, 21 19, 22, 23 19, 21, 22 16, 17, 20 15, 17, 19
doi:10.1371/journal.pone.0144505.t002
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 7/16
to the baseline values, the IOP increased by 25 ± 16% (median: 25%; range: 3%, 60%) in the
control group and by 23 ± 12% (m edian: 21%; range: 2%, 46%) in the glaucoma group. All eyes
showed an increase in IOP during the pose.
Similar results were obtained if only one eye per individual was included into the statistical
analysis. Multilevel MELM results (Table 3, interaction ‘Pose
Time’) showed that the increase
in IOP from baseline was significant (P<0.001) for all yoga poses in the glaucoma group as
well as in the control group immediately at the start of the pose and 2 minutes into the pose.
The IOP then tended to return to baseline values immediately after assuming a seated position
and 10 minut es later in a seated position (P> 0.05 in most cases). Nonetheless, overall changes
in IOP values between the glaucoma group and the control group were not statistically signifi-
cant (P = 0.813). The interaction term ‘Group
Time
Pose’ reveals that the glaucoma group had
higher IOP measurements at the start and 2 minutes into the Uttanasana pose when compared
to controls (P = 0.017 and 0.098, respectively).
Tables 4 and 5 and Figs 8 and 9 show the results of the analysis of margins and contrasts for
the predictors pose, diagnostic group, and time. Even though IOP changed at different time
points (significantly when comparing immediately at the start of the pose and 2 minutes into
the pose vs. baseline), these changes did not differ significantly between glaucoma and healthy
eyes (although glaucoma eyes had IOPs 1 to 2 mmHg higher on average). This is also shown in
Fig 8. Table 5 shows that poses Adho Mukha Svanasana and Uttanasana on average led to
higher IOP increases than the other two and suggest that no carry-over effect occurred even
though the poses were not performed in a random sequence. This is also shown in Fig 9. Lastly,
Fig 5. Least squares means and mean values of the covariates of the changes in IOP in the
Uttanasana position over time. The X axis represents each time point an IOP measurement was taken
(0 = Baseline seated; 1 = Immediate position; 2 = 2 minutes position; 3 = Post position seated; and 4 = 10
minutes post position seated). The Y axis represents the IOP in mmHg after adjusting for the covariates.
Subjects with glaucoma diagnosis are depicted ‘Glaucoma = 1’; controls are ‘Glaucoma = 0’.
doi:10.1371/journal.pone.0144505.g005
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 8/16
body mass index and age were not significantly associated with IOP changes for any yoga posi-
tion (Table 3).
Discussion
We tested the hypothesis that changes in body position during yoga lead to changes in IOP
among both healthy and POAG subjects. We confirmed the hypothesis and observed that the
position-associated IOP changes occurred immediately within one to two minutes after assum-
ing the position, returning to values close to baseline after assuming a seated position and 10
minutes later in a seated position. Glaucoma diagnosis did not show a significant effect on IOP
increase and poses Adho Mukha Svanasana and Uttanasana were associated with greater IOP
elevation.
Both normal and glaucoma subjects showed a rise in IOP in all four yoga positions. Inde-
pendent of the position, the rise ranged between 6 mmHg and 11 mmHg. It occurred within
one minute after assuming the body position of the yoga exercise, and the IOP returned to the
baseline values within two minutes after again being seated, with no further significant changes
thereafter. The results suggest that all individuals experience an acute elevation in IOP immedi-
ately after assuming certain common yoga positions. This rise in IOP lasts as long as the exer-
cise takes place, and the IOP returns to the baseline values shortly after sitting. The duration of
the yoga pose was two minutes.
Our results agree with those of previous studies and case reports which tested only the head-
stand position and which showed a marked two-fold rise in IOP.[16, 21, 22] Our study extends
Fig 6. Least squares means and mean values of the covariates of the changes in IOP in the Halasana
position over time. The X axis represents each time point an IOP measurement was taken (0 = Baseline
seated; 1 = Immediate position; 2 = 2 minutes position; 3 = Post position seated; and 4 = 10 minutes post
position seated). The Y axis represents the IOP in mmHg after adjusting for the covariates. Subjects with
glaucoma diagnosis are depicted ‘Glaucoma = 1’; controls are ‘Glaucoma = 0’.
doi:10.1371/journal.pone.0144505.g006
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 9/16
those findings to show that other yoga exercises with a head down position can lead to a rapid
and profound elevation in IOP. The measurements obtained in our study also revealed that the
yoga position associated rise in IOP occurred within one minute after taking the position and
that, in a similar manner, the IOP returned to the pre-exercise values within two minutes after
being seated.
In previous studies, the evaluat ion of IOP and body position typically used a fixed measure-
ment sequence. We used the Reichert Model 30 Pneumatonometer in a baseline, immediate, 2
minute, post, and 10 minute sequence for each position. This presents difficulties in interpreta-
tion because IOP measurements are affected by the measurement sequence. This applies due to
multiple IOP measurements being taken in a short period of time and repeated measurements
of IOP can result in a decrease in the readings. [24–26]
As a result of multiple IOP measurements, the magnitude of the changes owing to body
position have been uncertain, with different studies reporting differences between sitting and
supine IOP ranging from 0.3 to 5.6 mmHg for normal and glaucoma subjects; the use of the
Mackey-Marg tonometer with calibration from a pneumatonograph and the Medtronic Model
30 Classic pneumatonometer were used for these data collections.[13, 27, 28] Through the
asana (yoga position) change analysis we identified changes in IOP during four standard poses
other than the previously studied sirsasana, in glaucoma and healthy control subjects. Inverted
positions increase IOP significantly, but common positions have been incompletely investi-
gated. Yoga practitioners may need to be aware of IOP changes duri ng common yoga
positions.
Fig 7. Least squares means and mean values of the covariates of the changes in IOP in the Viparita
Karani position over time. The X axis represents each time point an IOP measurement was taken
(0 = Baseline seated; 1 = Immediate position; 2 = 2 minutes position; 3 = Post position seated; and 4 = 10
minutes post position seated). The Y axis represents the IOP in mmHg after adjusting for the covariates.
Subjects with glaucoma diagnosis are depicted ‘Glaucoma = 1’; controls are ‘Glaucoma = 0’.
doi:10.1371/journal.pone.0144505.g007
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 10 / 16
Table 3. Analysis of a Mixed-Effects Regression between the Change in Intraocular Pressure and Various Parameters during Yoga Exercises with
Head-Down Positions.
IOP Coef. 95% Conf. Interval P-value
Time 0.28 -0.05 0.61 0.095
Age -0.01 -0.06 0.03 0.545
BMI -0.01 -0.16 0.13 0.86
Group: Glaucoma 0.32 -2.35 2.99 0.813
Pose Reference:
Adho Mukha Svasana (1)
Uttanasana (2) 1.13 -1.27 3.52 0.357
Halasana (3) 0.59 -1.87 3.05 0.637
Viparita Karani (4) 0.3 -2.09 2.69 0.806
Group*Pose
12 -0.68 -4.16 2.8 0.701
13 0.74 -2.79 4.26 0.682
14 0.44 -2.99 3.88 0.8
Time Reference:
Baseline (0)
1 11.02 9.98 12.06 <0.001
2 11.61 10.62 12.61 <0.001
3 0.43 -0.61 1.47 0.415
4 0
Group*Time
11 -0.94 -2.63 0.75 0.276
12 -0.98 -2.72 0.76 0.268
13 -0.53 -2.34 1.29 0.571
14 -0.68 -2.6 1.24 0.487
Pose*Time
21 -4 -5.64 -2.36 <0.001
22 -4.1 -5.79 -2.41 <0.001
23 -1.18 -2.94 0.59 0.192
24 -0.8 -2.67 1.07 0.401
31 -7.22 -8.9 -5.53 <0.001
32 -7.73 -9.47 -5.99 <0.001
33 -1.91 -3.73 -0.1 0.039
34 -2.07 -3.99 -0.15 0.035
41 -7.78 -9.42 -6.13 <0.001
42 -9.25 -10.94 -7.56 <0.001
43 -1.48 -3.24 0.29 0.102
44 -1.68 -3.54 0.19 0.079
Group*Pose*Time
121 2.92 0.53 5.3 0.017
122 2.07 -0.38 4.53 0.098
123 1.2 -1.36 3.77 0.358
124 0.52 -2.19 3.24 0.706
131 1.77 -0.65 4.19 0.151
132 1.48 -1.01 3.97 0.243
133 1.39 -1.21 3.99 0.296
134 1.54 -1.21 4.29 0.272
(Continued)
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 11 / 16
The yoga pose-associated rise in IOP may be explained by the hydrostatic increase in the
pressure of episcleral veins and orbital veins into which aqueous humor is eventually drained
and the pressures of which directly influence the IOP according to the Goldmann equation,
Po = (F/C) + Pv, where Po is the IOP in mmHg, F is the rate of aqueous formation, C is the
facility of outflow, and Pv is the episcleral venous pressure. Another factor which may poten-
tially be involved in position-associated IOP changes may be changes in choroidal thickness.
The choroid is drained through the vortex veins, which continue into the superior ophthalmic
vein and finally into the intracranial cavernous sinus. Body position-associated changes in the
intracranial cerebrospinal fluid pressure (CSFP) may thus indirectly influence the venous pres-
sure in the choroid and the choroidal thickness and volume.[29]
Since elevated IOP is the most important known risk factor for development and progres-
sion of glaucomatous optic neuropathy, the rise in IOP after assuming the yoga poses is of con-
cern for glaucoma patients. It has remained elusive whether the concomitant rise in
cerebrospinal fluid pressure as the trans-lamina cribrosa counter-pressure against the IOP suf-
ficiently compensates in amount in a timely manner for the rise in IOP. This study can there-
fore neither warn glaucoma patients not to perform yoga poses with head-down positions nor
negate the possibility of exacerbating glaucomatous damage when performing yoga exercises
with head-down positions.
Potential limitations of our study should be mentioned. First, the glaucoma group was sig-
nificantly older than the non-glaucom atous group, so the comparison between both groups in
the yoga pose -associated change in IOP should be cautiously interpreted. We minimized this
effect by including age as a covariate in the multivariate analysis. Second, blood pressure was
not measured; thus no information was obtained which could point to associated changes in
cerebrospinal fluid pressure due to yoga position. Third, the duration of each pose was <5 min-
utes, therefore the study design does not allow conclusions on the change in IOP if yoga posi-
tions are kept for 30 minutes or an hour, such as in a formal yoga setting or class. Fourth, the
number of study participants was relatively small, which could help explain the lack of
Table 3. (Continued)
IOP Coef. 95% Conf. Interval P-value
141 0.79 -1.57 3.14 0.512
142 0.83 -1.59 3.25 0.502
143 0.88 -1.66 3.41 0.498
144 0.81 -1.87 3.48 0.555
P<0.01 denotes statistical significance.
doi:10.1371/journal.pone.0144505.t003
Table 4. Analysis of margins and contrasts for the predictors pose, diagnostic group, and time.
IOP
Group@Time Contrast Std. Err. z P>|z| [95% Conf. Interval]
(1 vs base) 0 0.4479324 0.8388864 0.53 0.593 -1.196255 2.092119
(1 vs base) 1 0.8784879 0.8410353 1.04 0.296 -0.769911 2.526887
(1 vs base) 2 0.5632102 0.8474495 0.66 0.506 -1.09776 2.224181
(1 vs base) 3 0.7889046 0.8580332 0.92 0.358 -0.8928095 2.470619
(1 vs base) 4 0.4847379 0.8726347 0.56 0.579 -1.225595 2.195071
doi:10.1371/journal.pone.0144505.t004
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 12 / 16
statistically significant differences between the glaucoma and the non-glaucoma groups in the
yoga associated IOP changes, and which does not necessarily suggest that there is no difference.
Absence of proof is not necessarily a proof of absence if the study sample is small. Future stud-
ies with a larger study sample may be needed to further explore the association of the IOP
changes in glaucoma and non-glaucoma groups. Fifth, in an attempt to keep a controlled order
for all subjects, the order of poses was not randomized. A randomized order of poses could be
analyzed in a future study. Such effects are likely to be minimal, as all IOPs went back to
Table 5. Analysis of margins and contrasts for the predictors pose, diagnostic group, and pose*time.
IOP- Pose@Time Contrast Std. Err. z P>|z| [95% Conf. Interval]
(2 vs base) 0 0.7847222 0.887311 0.88 0.376 -0.9543754 2.52382
(2 vs base) 1 -1.756944 0.8913703 -1.97 0.049 -3.5033998 -0.0098908
(2 vs base) 2 -2.279167 0.9034386 -2.52 0.012 -4.049874 -0.5084595
(2 vs base) 3 0.2111111 0.9232021 0.23 0.819 -1.598332 2.020554
(2 vs base) 4 0.2458333 0.9501805 0.26 0.796 -1.616486 2.108153
(3 vs base) 0 0.9608382 0.8990916 1.07 0.285 -0.8013489 2.723025
(3 vs base) 1 -5.369717 0.9032031 -5.95 0 -7.139963 -3.599472
(3 vs base) 2 -6.02944 0.9154268 -6.59 0 -7.823643 -4.235236
(3 vs base) 3 -0.2599951 0.9354448 -0.28 0.781 -2.093433 1.573443
(3 vs base) 4 -0.3377729 0.9627709 -0.35 0.726 -2.223769 1.549223
(4 vs base) 0 0.5223753 0.8759818 0.6 0.551 -1.194518 2.239268
(4 vs base) 1 -6.85818 0.8799854 -7.79 0 -8.58292 -5.133441
(4 vs base) 2 -8.312347 0.8918883 -9.32 0 -10.06042 -6.564278
(4 vs base) 3 -0.5151247 0.911381 -0.57 0.572 -2.301399 1.271149
(4 vs base) 4 -0.7498469 0.9379905 -0.8 0.424 -2.588275 1.088581
doi:10.1371/journal.pone.0144505.t005
Fig 8. Predictive Margins of Diagnostic Groups versus Time with 95% Confidence Intervals.
doi:10.1371/journal.pone.0144505.g008
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 13 / 16
baseline before performing the next pose. The significance of variables such as age and body
mass index should be interpreted with caution. Seventh, the design of our study did not allow
examining changes in cerebrospinal fluid pressure (CSFP) during the yoga poses or examining
a progression of glaucoma during the yoga poses and when yoga exercises are often performed.
The purpose of our investigation was to assess whether, when and for which amount of IOP
changes occur during yoga poses in normal individuals and in glaucoma patients. Despite the
relatively small sample size, the results appear to be clear that in normal and in glaucoma
patients, the IOP increases rapidly after taking the poses and re-normalizes rapidly as soon as
the yoga exer cises end. Future studies may now be warranted to further elucidate the interplay
of IOP increase and the increase in CSFP and to assess whether yoga poses are a risk for glau-
coma patients. Based on the results of the present study, one may state that glaucoma patients
(as normal individuals) do experience an increase in IOP as soon as they hold a head-down
yoga pose, and that that may be of potential risk for a glaucomatous optic nerve. The main
value of the study is that it may have suggested in a qualitative manner as a proof of principle
that the IOP rapidly adjusts to acute changes in body position. It raises new questions and
potentially initiates larger-scaled studies on which parameters these IOP changes depend,
including factors such as the speed of change in body position, duration of staying in the new
body position, and associated changes in blood pressure, jugular vein pressure and in episcleral
venous pressure.
In conclusion, normal subjects and open-angle glaucoma subje cts experienced a statistically
significant and rapid increase in IOP shortly after starting yoga exercises with head-down posi-
tions. In a similar manner, IOP dropped shortly after stopping the yoga exercises. Future stud-
ies may address whether the yoga pose associated rise in IOP markedly differs between
glaucoma patients and normal individuals and if yoga practitioners performing these positions
for a longer time period will have a longer duration of IOP rise. Although elevated IOP is a
major risk factor for glaucomatous optic neuropathy, it remains unclear whether the yoga pose
Fig 9. Predictive Margins of Yoga Pose versus Time with 95% Confidence Intervals.
doi:10.1371/journal.pone.0144505.g009
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 14 / 16
with head-down position associated with a rise in IOP increases the risk of progression among
glaucoma patients.
Supporting Information
S1 TREND Checklist. TREND Checklist.
(PDF)
S1 Protocol. Protocol.
(DOC)
Author Contributions
Conceived and designed the experiments: JVJ JBJ CGDM RR. Performed the experiments: JVJ
JBJ CGDM RR. Analyzed the data: JVJ JBJ CGDM RR. Contributed reagents/materials/analysis
tools: JVJ JBJ CGDM RR. Wrote the paper: JVJ JBJ CGDM RR.
References
1. Tarkkanen A, Leikola J. Postural variations of the intraocular pressure as measured with the Mackay-
Marg tonometer. Acta ophthalmologica. 1967; 45(4):569–75. PMID: 6072270
2. Klatz RM, Goldman RM, Pinchuk BG, Nelson KE, Tarr RS. The effects of gravity inversion procedures
on systemic blood pressure, intraocular pressure, and central retinal arterial pressure. The Journal of
the American Osteopathic Association. 1983; 82(11):853–7. PMID: 6885535
3. LeMarr JD, Golding LA, Adler JG. Intraocular pressure response to inversion. American journal of
optometry and physiological optics. 1984; 61(11):679–82. PMID: 6517124
4. Buchanan RA, Williams TD. Intraocular pressure, ocular pulse pressure, and body position. American
journal of optometry and physiological optics. 1985; 62(1):59–62. PMID: 3976837
5. Hirooka K, Shiraga F. Relationship between postural change of the intraocular pressure and visual field
loss in primary open-angle glaucoma. Journal of glaucoma. 2003; 12(4):379–82. PMID: 12897586
6. Prata TS, De Moraes CG, Kanadani FN, Ritch R, Paranhos A Jr. Posture-induced intraocular pressure
changes: considerations regarding body position in glaucoma patients. Survey of ophthalmology.
2010; 55(5):445–53. doi: 10.1016/j.survophthal.2009.12.002 PMID: 20637484
7. Wilensky JT. Diurnal variations in intraocular pressure. Transactions of the American Ophthalmological
Society. 1991; 89:757. PMID: 1687295
8. Anderson DR, Grant WM. The influence of position on intraocular pressure. Investigative ophthalmol-
ogy. 1973; 12(3):204–12. PMID: 4692261
9. Weber AK, Price J. Pressure differential of intraocular pressure measured between supine and sitting
position. Annals of ophthalmology. 1981; 13(3):323–6. PMID: 7258940
10. Tsukahara S, Sasaki T. Postural change of IOP in normal persons and in patients with primary wide
open-angle glaucoma and low-tension glaucoma. British journal of ophthalmology. 1984; 68(6):389–
92. PMID: 6722071
11. Carlson KH, McLaren JW, Topper JE, Brubaker RF. Effect of body position on intraocular pressure and
aqueous flow. Investigative ophthalmology & visual science. 1987; 28(8):1346–52.
12. Mosaed S, Liu JH, Weinreb RN. Correlation between office and peak nocturnal intraocular pressures in
healthy subjects and glaucoma patients. American journal of ophthalmology. 2005; 139(2):320–4.
PMID: 15733994
13. Weinreb RN, Cook J, Friberg TR. Effect of inverted body position on intraocular pressure. American
journal of ophthalmology. 1984; 98(6):784–7. PMID: 6507552
14. Friberg TR, Sanborn G. Optic nerve dysfunction during gravity inversion. Pattern reversal visual evoked
potentials. Archives of ophthalmology. 1985; 103(11):1687–9. PMID: 4062635
15. Linder BJ, Trick GL, Wolf ML. Altering body position affects intraocular pressure and visual function.
Investigative ophthalmology & visual science. 1988; 29(10):1492–7.
16. Baskaran M, Raman K, Ramani KK, Roy J, Vijaya L, Badrinath SS. Intraocular pressure changes and
ocular biometry during Sirsasana (headstand posture) in yoga practitioners. Ophthalmology. 2006; 113
(8):1327–32. PMID: 16806478
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 15 / 16
17. Kiuchi T, Motoyama Y, Oshika T. Relationship of progression of visual field damage to postural
changes in intraocular pressure in patients with normal-tension glaucoma. Ophthalmology. 2006; 113
(12):2150–5. PMID: 16996611
18. Bertschinger DR, Mendrinos E, Dosso A. Yoga can be dangerous—glaucomatous visual field defect
worsening due to postural yoga. The British journal of ophthalmology. 2007; 91(10):1413–4. PMID:
17895421
19. Saper RB, Eisenberg DM, Davis RB, Culpepper L, Phillips RS. Prevalence and patterns of adult yoga
use in the United States: results of a national survey. Alternative Therapies In Health And Medicine.
2004; 10(2):44–9. PMID: 15055093
20. Cramer H, Krucoff C, Dobos G. Adverse events associated with yoga: a systematic review of published
case reports and case series. PloS one. 2013; 8(10):e75515. doi: 10.1371/journal.pone.0075515
PMID: 24146758
21. Gallardo MJ, Aggarwal N, Cavanagh HD, Whitson JT. Progression of glaucoma associated with the Sir-
sasana (headstand) yoga posture. Advances in therapy. 2006; 23(6):921–5. PMID: 17276961
22. Monteiro de Barros DS, Bazzaz S, Gheith ME, Siam GA, Moster MR. Progressive Optic Neuropathy in
Congenital Glaucoma Associated with the Sirsasana Yoga Posture. Ophthalmic Surgery, Lasers, and
Imaging. 2008; 39(4):339–40.
23. Pettinato Y. Simply Yoga. Hinkler Books Pty, Limited2002. p. 22–3.
24. Almubrad TM, Ogbuehi KC. On repeated corneal applanation with the Goldmann and two non-contact
tonometers. Clinical & experimental optometry: journal of the Australian Optometrical Association.
2010; 93(2):77–82.
25. Gaton DD, Ehrenberg M, Lusky M, Wussuki-Lior O, Dotan G, Weinberger D, et al. Effect of repeated
applanation tonometry on the accuracy of intraocular pressure measurements. Current eye research.
2010; 35(6):475–9. doi: 10.3109/02713681003678824 PMID: 20465440
26. Jóhannesson G, Hallberg P, Eklund A, Behndig A, Lindén C. Effects of topical anaesthetics and
repeated tonometry on intraocular pressure. Acta ophthalmologica. 2014; 92(2):111–5. doi: 10.1111/
aos.12058 PMID: 23387522
27. Jain MR, Marmion VJ. Rapid pneumatic and Mackey-Marg applanation tonometry to evaluate the pos-
tural effect on intraocular pressure. The British journal of ophthalmology. 1976; 60(10):687–93. PMID:
1009040
28. Sit AJ, Nau CB, McLaren JW, Johnson DH, Hodge D. Circadian variation of aqueous dynamics in
young healthy adults. Investigative ophthalmology & visual science. 2008; 49(4):1473–9.
IOP Rise in Subjects with and without Glaucoma during Yoga
PLOS ONE | DOI:10.1371/journal.pone.0144505 December 23, 2015 16 / 16
