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General Review

Reductions in Intraocular Pressure After Acute Aerobic Exercise: A Meta-Analysis

Roddy, Gabrielle MA; Curnier, Daniel PhD; Ellemberg, Dave PhD

Author Information
Clinical Journal of Sport Medicine: September 2014 - Volume 24 - Issue 5 - p 364-372
doi: 10.1097/JSM.0000000000000073
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Abstract

INTRODUCTION

Primary open-angle glaucoma (POAG) is a disease of the eye that progresses asymptomatically for many years, until visual deficits and irreversible damage to the retina have already occurred.1 It is the second leading cause of blindness worldwide and will affect 80 million people by the year 2020.1 Complementary lifestyle changes alongside clinical treatment of POAG are becoming increasingly important as prevalence of the disease increases coupled with decreasing access to eye health care for low-income, elderly populations.2 Of the many implicated risk factors, including age, heredity, and corneal thickness, elevated intraocular pressure (IOP) remains the only controllable risk factor for POAG.3–5 Exercise is a significant factor in the prevention and management of many chronic and age-related diseases, and the literature on the relationship between exercise and IOP spans over 5 decades.6,7 Although studies vary widely with regard to population descriptions and exercise protocol, the majority show a transient reduction in IOP after acute aerobic exercise.6,7

Normal IOP levels are generally thought to range from 11 to 21 mm Hg, and clinically high IOP is often differentiated by repeated readings over 21.0 to 24.0 mm Hg.5,8,9 The majority of studies on the effect of aerobic exercise on IOP find reductions from preexercise values on the order of 1.4 to 8.0 mm Hg in sedentary and normally active populations.6,7,10,11

Acute aerobic exercise produces transient reductions in IOP across intensity levels that range from light to moderate, such as a brisk walk and vigorous running on a treadmill, to volitional exhaustion on treadmills or cycle ergometers.7 There is evidence that it is exercise intensity alone and not exercise duration that is the key factor involved in the magnitude of the reduction in IOP.12–15 A qualitative comparison of results across studies suggests that the relationship between the intensity of aerobic exercise and IOP is not entirely clear. Field running for 15 minutes13 and walking for 13.5 minutes10 in normally active participants produce reductions in IOP of 4.3 and 1.4 mm Hg, respectively. There is a nominal difference in duration between the 2 conditions, but running produces the greater reduction in IOP.16,17 An even higher intensity exercise, such as running up and down 7 flights of stairs, also produces a reduction of 4.3 mm Hg.18 These results suggest a possible ceiling effect, a level beyond which exercise intensity no longer impacts the magnitude of reduction in IOP.

Another factor affecting postexercise IOP is the current fitness profile of a participant. A greater reduction is observed in sedentary populations when compared with those who are physically active.7,12,19 Harris et al12 compared 2 groups of participants divided a posteriori into sedentary and active groups by the concentration of lactate (lactic acid that has diffused out of the muscle) in the bloodstream after a vigorous 10-minute session on a cycle ergometer.20,21 When the results were stratified, the sedentary group experienced an almost 2-fold reduction in IOP as compared with the active group (−4.7 vs −2.7 mm Hg, respectively).12

The current meta-analysis was designed to obtain a quantitative estimate of the overall effect of acute aerobic exercise on IOP and also the relative contributions of exercise intensity and duration, and the degree to which these variables affect sedentary and normally active populations. For those populations most at risk for the development of POAG, it is important to examine the potential of aerobic exercise as a factor in the management of continued eye health.5

MATERIALS AND METHODS

Search Strategy

An open search was performed on the electronic databases PubMed from 1977, Web of Science from 1979 (including MEDLINE from 1950), and Embase from 1974, through to March 2, 2012.

The Cochrane List of Registered Trials and the archived abstracts from the annual meetings of the Association for Research in Vision and Ophthalmology and the Vision Sciences Society, from 2001 to the present, were also searched for unpublished studies. The references of relevant studies were hand searched. The keywords used in a pilot search of PubMed for related literature were physical activity or exercise* AND intraocular pressure OR ocular blood flow OR ocular tension OR glaucoma. For the final search, the MeSH (PubMed), EMTREE (Embase), and free-text keywords such as “exercise*” and “intraocular pressure” were used.

Identification of Studies

The search yielded 658 articles as follows: PubMed (n = 188), Web of Science/Medline (n = 230), and Embase (n = 240) including 355 duplicates. Of the remaining studies, 268 were excluded by abstract (Figure 1). There were no relevant unpublished studies found during the search that matched the criteria of this analysis. There were 35 potentially relevant published sources from which 2 were excluded because the results pertaining to a specific set of participants were used in a previous publication. Nineteen studies were excluded because of missing statistical information that could not be obtained from the authors contacted (n = 8). Ten studies were included in this meta-analysis, producing 14 independent groups (Table 1).

FIGURE 1
FIGURE 1:
Flow chart of study selection and criteria for exclusion.
TABLE 1
TABLE 1:
General Characteristics of Participants

An independent reviewer (D.E.) was consulted for all questions regarding inclusion of a potentially relevant study.

Inclusion Criteria

The following inclusion criteria were imposed:

  1. Studies must include postexercise ΔIOP measured after the first acute bout of aerobic exercise on a given test day and associated SD or standard error (SE) or raw participant data.
  2. Participants should be sedentary, normally active, or athletic (excluding professional athletes) displaying no preexisting ocular pathologies or IOP more than 18 mm Hg.
  3. To reduce the likelihood of age-related pathologies that may affect the eye, all participants should not be older than 55 years of age.25,26
  4. Exercise should be aerobic in nature and the intensity must be quantifiable using physiological target measures such as a percentage of
  5. (a measure of maximal oxygen uptake) or a submaximal estimation of maximum heart rate (MHR).
  6. Exercise should be no less than 2 minutes, ensuring at least partial recruitment of the aerobic system and no more than 60 minutes within daylight hours to constrain the effect of diurnal variation.27,28

Assessment of Risk and Bias

Of potential studies to be included in this analysis, only those of Harris et al12 and Passo et al22 were included in the Cochrane Register of Controlled Trials.29 In both cases, only a subset of the conditions could be included. Therefore, the evaluation tool for assessing the risk of bias was not used.

Data Extraction

The following information was extracted from each study: postexercise ΔIOP (measured in mm Hg) and associated variance, participant characteristics, type and duration of exercise, physiological and absolute measures of exercise intensity, IOP measurement methodology and tools, latency of the postexercise measure, authors, date and country of publication, and any information pertaining to the control of covariates.

Outcome Variables

The primary outcome variable to be examined in this analysis was postexercise ΔIOP. The relative contribution of exercise intensity and duration to the relationship between exercise and IOP, and their differential effects on each population were also evaluated.

To standardize the energy cost of the exercises across studies, physiological markers of intensity were converted to a metabolic equivalent of task (MET; Table 2). For studies using a submaximal percentage of

as the target training range, the standard formula for conversion from

to a MET value was applied [%

(mL·kg−1·min−1)/3.5].19,22,30(p162) Four studies required a conversion of the given sub-MHR to a percentage of

for which we used a linear regression [% MHR = 0.646 × (%

× 100) + 37.182]31 followed by conversion to a MET value as above.11,13,15,24 Where necessary, MET values were weighted for sex using

normative tables for females and males between 20 and 29 years of age in the 50th percentile.11,19,24,32 For the remaining studies,10,12,18,23 MET values were assigned using the 1993 and 2011 Compendia of Physical Activities.16,17

TABLE 2
TABLE 2:
Study Descriptions

Statistical Analyses

Assuming that all studies were not functionally equivalent, random effects model was used to produce subgroup analyses and a forest plot. Meta-regressions were used to verify the impact of group allocation, intensity, and duration on the interstudy variability of the effect size (ES). Analyses were done with Stata version 12.1 (StataCorp, Durham University, United Kingdom) using a significance level of 5%.

RESULTS

Search Results

Participant Characteristics

The combined studies produced 231 participants of whom 67 were female and 130 were male (Table 1). The sex of 34 participants was not specified.12,18 The normally active group includes all participants described as trained, athletic, or otherwise normally active (n = 124).

Study Characteristics

Four studies produced 2 independent groups each (Table 1). The preconditioning results from both the experimental and control groups in the long-term study by Qureshi23 are included as 2 sedentary groups. In the study by Karabatakis et al,11 the results from a single group including “untrained” and “athletic” participants were divided into a sedentary group (group U, n = 4) and a normally active group (group A, n = 25). The 2 groups in the “fixed” intensity condition from Harris et al12 and both the sedentary and the athletic groups from Dane et al19 were included in this analysis. The preconditioning results from all 10 participants included in study of Passo et al22 were included in this analysis as a single sedentary group.

Two of the studies included in this analysis tested different intensity conditions in a within-subjects design (Table 2). From the study by Qureshi et al,15 we included only the 15-minute, 60% MHR condition in the current analysis. From the study by Kiuchi et al,13 the 15-minute, 70% MHR condition was included in this analysis. These conditions represented a duration and intensity not included in other studies.

Statistical Results

The current meta-analysis reveals that there is a significant effect of exercise on postexercise IOP [unstandardized ES = −3.263; confidence interval (CI), −4.158 to −2.368; P < 0.001; Figure 2]. When the ES is stratified by group allocation, both the sedentary group (ES = −4.198; CI, −5.151 to 3.245) and the normally active group (ES = −2.340; CI −3.305 to −1.375) are significantly different than zero (P < 0.000; Figure 2; Table 3). Group allocation (sedentary vs normally active) contributes significantly to the overall ES (B = −1.886; SE = 0.818; P = 0.043) and explains 27.60% (

) of the between-study variability (Table 4). The residual between-study variability is estimated by tau2 (T2) in the same metric as the ΔIOP (in mm Hg). Group allocation produced a T2 of 2.009 (Table 4). The I2 value of 89% should be interpreted as the proportion of residual variability actually attributed to between-study heterogeneity (T2), whereas the remaining 11% of the between-study variability assumes within-study sampling error.33

Figure
Figure
TABLE 3
TABLE 3:
Tests of Heterogeneity
TABLE 4
TABLE 4:
The Contribution of Group, Intensity, and Duration to the Overall ES and Differential Group Responses to Those Variables

To quantify the contribution of intensity (METs) and duration (in minutes) of exercise to the overall ES, a separate regression was performed for each because there were not enough studies to include all variables in a single meta-regression. There was no significant contribution to the overall ES for these 2 factors (B = 0.105; SE = 0.177; P = 0.562 or B = −0.031; SE = 0.026; P = 0.252; Table 4). To analyze whether group differences can be explained by the response of each group to intensity or duration of exercise, we controlled for the variables 1 at time and added group allocation in a sequential multiple meta-regression. In all cases, group allocation remainded significant, whereas intensity and duration of exercise remained nonsignificant (Table 4).

DISCUSSION

Over the past 5 decades, a large number of empirical studies investigated the relationship between acute aerobic exercise and IOP. However, researchers often neglect to report the variance associated with the mean change in IOP after exercise, without which the results cannot be interpreted given the small sample sizes in many studies. Furthermore, exercise intensity and duration are quantified differently across studies. The objective of the current work was to combine the results of studies that looked specifically at the effect of acute aerobic exercise on IOP, to obtain greater statistical power, and to verify the influence of the key factors implicated in the relationship between aerobic exercise and IOP. The results of this analysis indicate that there is a significant effect of an acute bout of aerobic exercise on postexercise IOP that is almost 2-fold greater for sedentary populations than for normally active populations (ES = −4.198 and −2.340, respectively; Figure 2). According to the available data, group differences cannot be explained by exercise intensity or duration (Table 4). However, given the heterogeneity across studies, it is important to consider the limitations of this analysis and the studies within before the clinical implications of these results can be explored.

Limitations of this Analysis and Included Studies

The difference in the methodology across studies is potentially reflected in the elevated I2 values (>88% across analyses; Tables 3 and 4). I2 can be thought of as the proportion of residual variability attributed to between-study heterogeneity (denoted by T2; Tables 3 and 4) as opposed to within-study sampling error.33 The methodological differences range from the determination of population and exercise parameters to the control of variables that cause IOP fluctuation beyond that which is caused by exercise.

The physical fitness of an individual participant has been posited as a factor in the magnitude of reduction in IOP that can be expected with exercise.19,22,23 Therefore, any ambiguity with regard to the parameters governing group allocation in the original study is compounded here and may affect the magnitude of the ES. By example, the normally active participants in the study by Dane et al19 produced a +0.33 mm Hg increase in IOP after exercise, as opposed to a decrease, and were likely at a higher level of fitness than the other normally active groups in this analysis.

In accord with the idea that there is an interaction between a participant's current fitness level and the effect of exercise on IOP, the magnitude of reduction in postexercise IOP is often found to be in proportion with relative intensity rather than absolute intensity measures.10,12,13,15,22 However, as the parameters governing acute exercise were notably different across studies, including supporting physiological data, the intensity measures from each study were converted to MET values, an absolute measure.30(pp4,5) The conversion to MET values allowed for comparison across all studies, and the ages of the participants were in a small range that would not bring too much weight to the higher end of the scale. In 9 of the 10 studies, participants ranged between 17 and 30 years of age, with the exception of the 10 participants in the study by Passo et al22 who were of approximately 37 years old. For clarity, stratification by relative intensity is compared with the assigned METs (Table 5). Although there is not enough statistical power, in any 1 group, to create a subgroup analysis by relative intensity category, Table 5 provides a clearer picture of how the MET values derived for each study compare with approximations of relative values and the nature of the discrepancies.

TABLE 5
TABLE 5:
Comparison of MET Values and Relative Intensity Categories

A qualitative analysis of the MET values assigned to each study reveals that when divided into 2 categories, moderate-intensity exercise (3-6 METS) or vigorous exercise (>6 METS),30(pp4,5) the difference in the average reduction in IOP is <1.0 mm Hg. The difference is also <1.0 mm Hg when the studies13,15,19,22 that straddle categories are all placed into the moderate category and when the anomalous study with a MET value of 1518 is removed entirely (Table 5). Regardless of the method of categorization, intensity does not bear weight on the outcome as per this analysis.

The control of covariates is paramount when embarking on an examination of the relationship between exercise and reductions in IOP because of physiological factors that cause IOP fluctuations, including posture,28 diurnal variation,27,28 smoking,34,35 and fluid intake.36,37 To control for fluctuations in posture, the exercise criteria of the included studies were constrained to walking, jogging, running, or cycling. Duration was constrained to 1 hour in the daytime to control for diurnal to nocturnal variation in IOP.28,34 However, a lack of information across studies did not allow the comparison of many other covariates. Preexercise fluid intake is a notable example as water, coffee, and alcohol have differential transient effects on IOP.18,36,37

The control of covariates is further complicated by the fact that postexercise measurements of IOP are subject to substantial variation across equipment, and within and across observers. Five studies included in this analysis used Goldmann applanation tonometery (GAT; Haag-Streit, Koeniz, Switzerland) (Table 2), the standard to which most other methods of IOP measurement are compared. The interobserver variability of GAT is 0.4 mm Hg and the 95% limit of agreement is ±2.6 mm Hg.38 However, GAT overestimates IOP in eyes with thicker corneas and underestimates IOP when corneas are thinner.39–41 The same is true for noncontact tonometry, used by 2 studies,10,18 which reads higher than GAT (mean difference from GAT ≈ 1.5 mm Hg; 95% limit of agreement ≈ ±3.0).40 The contact pneumotonometer used in the study by Dane et al19 has a mean difference of 0.72 ± 2.82 mm Hg from GAT,41 and the dynamic contour tonometry, used by Read and Collins24 has a mean difference of +1.7 mm Hg from GAT.42 It is not only the equipment but also the number of IOP measurements that can affect the outcome of a study. Repeated measurements with contact tonometers can reduce IOP by increasing outflow of the aqueous humor from the eye.39,41

The above factors contribute to substantial variations in the outcome of a given study and must be kept in mind when interpreting the results of the current analysis. Other factors that may impact IOP, such as sex and race, are not addressed in this analysis because there was not enough literature addressing these issues. Notwithstanding the above limitations, there is a robust effect of exercise on IOP that bears further examination.

Initial Observations

Intensity of Exercise

Contrary to much of the literature,12,13,15,43 intensity did not contribute significantly to the effect of aerobic exercise on IOP in the current analysis (Table 4). Neither could the difference in the magnitude of reduction in IOP between the sedentary and normally active groups be explained by their differential response to intensity (Table 4). This is a surprising finding as 2 of the groups included in this analysis were from studies that found that the magnitude of reduction in IOP was roughly proportional to relative intensity in a within-subjects design.13,15

As previously mentioned, the highest intensity exercise in this analysis, a 2-minute stair run at 15 METs,18 created the same reduction in a normally active population (4.34 mm Hg) as did a 15-minute run at 6.2 METs.13 This suggests a ceiling effect on the magnitude of reduction that can be expected with exercise for normally active participants regardless of the intensity. This is in accord with the study by Dane et al19 who showed that the physically fit participants experienced almost no change in IOP as compared with the sedentary group. Furthermore, in their studies on the change in IOP after long-term training, Passo et al22 and Qureshi23 showed that reductions in IOP were significantly less in the trained groups as compared with the control subjects.

Duration of Exercise

Like intensity, exercise duration did not significantly contribute to the effect of exercise on IOP. It should be noted that of the 10 included studies, 6 used exercise durations of 10 to 15 minutes (Table 2). The 3 sedentary groups from that subset produced an average reduction in IOP of 4.70 mm Hg.12,15,22 The 2 sedentary groups that exercised for 60 minutes produced an average reduction of 4.28 mm Hg.23 To examine whether it is the overall output of energy that dictates the magnitude of reduction in IOP rather than either intensity or duration alone, exercise intensity is expressed as product of the METs and the duration in minutes.44 Comparing these 2 subsets, we find that 60 minutes of cycling at 4.8 METs is more than 3 times the average quantity of the other 3 sedentary groups, yet the average reduction in IOP is slightly less. It seems that duration and intensity interact equivocally across studies.

Mechanisms

It remains unclear as to what mechanism contributes to the initial reduction in IOP after acute aerobic exercise. Changes in colloid osmotic pressure (a factor in capillary fluid exchange); increases in plasma osmolarity, ocular blood flow, and blood lactate; and decreases in blood pH have all been suggested as possible mechanisms that initiate a reduction in IOP.12,13,37,45–49 Loss of water and electrolytes by means of sweat during exercise cause increased plasma osmolarity, changes in colloid osmotic pressure, and ultimately dehydration.37,48,50(p892) However, duration did not contribute to the effect of exercise in this analysis, as one might expect if increasing dehydration were to play a role in the reduction of IOP.12 Furthermore, significant reductions in IOP were found after aerobic exercise of 5 minutes and less14,18,19 that are on par with the reductions produced at much longer durations.45

Some population-based studies report an association between systemic blood pressure and fluctuations in IOP.25,51,52 Although exercise is known to increase systolic blood pressure through sympathetic stimulation, it is less clear how that relationship relates to mechanisms involved in postexercise reductions in IOP. Five studies included in our analysis find no linear correlation between blood pressure and postexercise reductions in IOP.11–13,22,23

Long-term Effects of Exercise

There is evidence that over time, continued exercise22,23,53 and physical labor in the workplace54 induce adaptations of the sympathetic nervous system that contribute to an overall reduction in baseline IOP. As humans acclimatize to progressive heat, they sweat more profusely, which increases the plasma volume and diminishes the loss of electrolytes, thereby maintaining plasma osmolarity.50(pp892,893)

Two studies included in the current analysis, those of Qureshi23 and Passo et al,22 found reductions in baseline IOP of 0.8 to 1.3 mm Hg after long-term exercise conditioning. Passo et al,22 in particular, found that pretraining acute exercise decreased IOP in sedentary participants by 41% from baseline. After 3 months of exercise conditioning, 3 days per week, acute exercise reduced IOP by 12% from baseline, a reduction that persisted for an average of 3 weeks in some participants.22 The combined evidence suggests an enduring effect of exercise on IOP that is in accord with the idea that those who are physically fit will maintain a baseline IOP that is lower than those who do not exercise.19,22,23,53,54 It remains unclear whether exercise can slow down the progressive elevation of IOP that is part of the normal aging process.26,55

Clinical Implications

The robust effect of exercise on IOP in the sedentary group in this analysis outlines the need to continue this research with elderly and clinical populations. Generally, research finds differential reductions in IOP, via exercise, in elderly populations, dependent on baseline IOP55,56 and reductions of up to approximately 12.0 mm Hg for clinical populations.14 Exercise could also impact the rate of visual field loss, which increases exponentially, with increasing IOP, in those patients with POAG.57,58 It should be noted that there is some controversy with regard to the effect of exercise on IOP in clinical populations. Studies including populations with advanced glaucoma, or other severe subtypes such as pigmentary dispersion glaucoma, have found increases in IOP and temporary vision loss after exercise of varied intensity.59,60 Although there is a known protective effect when IOP is pharmacologically reduced immediately after diagnoses, only 60% to 70% of patients comply with long-term drug regimens because of the slow progression of the disease and negative side effects of the medication.61–63 Furthermore, population screening outside the health care system is not cost-effective, and many people are not diagnosed until noticeable symptoms bring them to consult their doctor.5,62

The possibility that exercise could be another useful tool in an eye health regimen is not a remote one. The Early Manifest Glaucoma Trial suggests that for every 1.0 mm Hg decrease in IOP, there is a 10% reduction in the rate of disease progression.34 Conversely, for every 1.0 mm Hg increase in IOP, there is a 19% increase in the progression of POAG.4 The target reduction in IOP in a clinical setting is often a stable reduction of 20% to 40% of baseline IOP.5,62,63 In the current analysis, the average baseline for the sedentary group is approximately 15 mm Hg, and the transient postexercise change in IOP is 4.198 mm Hg, a 28% reduction. Future research needs to concentrate on whether that transient postexercise reduction can be stabilized with the introduction of a regular aerobic exercise program.

CONCLUSIONS

The current analysis brought together studies that looked specifically at a single bout of aerobic exercise and postexercise change in IOP. There is a clear effect of aerobic exercise on IOP, most importantly for the sedentary group (ES = 4.198 mm Hg) as compared with the normally active group (ES = 2.340 mm Hg). The differential effect of exercise between the 2 groups is not explained by exercise intensity or duration. There are a number of limitations in this study, largely related to the sheer number of variables that affect transient changes in postexercise IOP and the variation in parameters across studies. Regardless, the magnitude of the overall postexercise change in IOP, for the sedentary group especially, suggests continued exploration into the usefulness of aerobic exercise as an additional factor in the management of continued eye health.

ACKNOWLEDGEMENTS

The authors acknowledge Miguel Chagnon for his invaluable statistics guidance.

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Keywords:

intensity; duration; sedentary; active; glaucoma prevention; physical activity

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