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Twenty-Four–Hour Pattern of Intraocular Pressure in the Aging Population

From the Departments of ¹ Ophthalmology and ² Psychiatry, University of California, San Diego, La Jolla, California.

	Abstract

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PURPOSE. To characterize the 24-hour pattern of intraocular pressure (IOP) in a sample of the aging human population.

METHODS. Twenty-one healthy volunteers 50 to 69 years of age were housed in a sleep laboratory for 24 hours. Experimental conditions were strictly controlled with a 16-hour light period and an 8-hour dark period. Sleep was encouraged in the dark period. Intraocular pressure was measured using a pneumatonometer every 2 hours (total of 12 times). Measurements were taken in both the sitting position and the supine position during the light/wake period but only in the supine position during the dark period.

RESULTS. When the sitting IOP data from the light/wake period and the supine IOP data from the dark period were considered, elevation and reduction of IOP occurred around the scheduled lights-off and lights-on transitions, respectively. Mean IOP in the dark period was significantly higher than mean IOP in the light/wake period. The trough appeared at the end of the light/wake period, and the peak appeared at the beginning of the dark period. The magnitude of trough-peak difference was 8.6 ± 0.8 mm Hg (mean ± SEM). Cosine fits of 24-hour IOP data showed a significant 24-hour rhythm. When IOP data from just the supine position were analyzed, the trough-peak IOP difference was 3.4 ± 0.7 mm Hg, with similar clock times for the trough and the peak. Cosine fits of supine IOP data showed no statistically significant 24-hour rhythm.

CONCLUSIONS. Nocturnal elevation of IOP occurred in this sample of the aging population. The trough of IOP appeared at the end of the light/wake period, and the peak appeared at the beginning of the dark period. The main factor in the nocturnal IOP elevation appeared to be the shift from daytime upright posture to supine posture at night.

	Introduction

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Ahigh intraocular pressure (IOP), usually determined during office hours, has been regarded as a major risk factor for glaucoma. The major type of glaucoma, open-angle glaucoma, affects mainly the aging population. There is insufficient information in the literature regarding the level of IOP at night in elder age groups including people suffering from glaucoma. Among the few reports,^{1 2 3 4 5} nocturnal IOP patterns in aging samples are inconsistent. Improving our knowledge of the basic 24-hour IOP pattern in the elderly would be beneficial to the diagnosis and treatment of glaucoma and related conditions, such as normal-tension glaucoma and ocular hypertension.

We recently described the 24-hour IOP patterns in two groups of young volunteers (18 to 25 years of age) housed in a sleep laboratory.⁶ Measurements of IOP were taken from these healthy volunteers at 2-hour intervals during a 16-hour light (wake) and 8-hour dark (sleep) period. Attention was given to the issues of light exposure and body position for IOP measurements. One group of volunteers that remained seated for the IOP measurement during the light/wake period and supine during the dark period (mimicking the natural day-night postures) showed a pronounced IOP elevation at night. A smaller nocturnal IOP elevation independent of postural influence was evident in the other group of volunteers, who remained in the supine position for all IOP measurements. The nocturnal IOP pattern in the aging population, as indicated in a previous report,⁵ might be different from that in the young adults. With the same approach applied to the young volunteers,⁶ we collected 24-hour IOP data from 21 healthy volunteers 50 to 69 years of age. The 24-hour IOP pattern in this aging sample was compared with patterns observed in the younger volunteers.

	Methods

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The study followed the tenets of the Declaration of Helsinki and was approved by the Institutional Review Board. Responding to newspaper and newsletter advertisements, 21 local residents (59.6 ± 6.3 years, mean age ± SD) were recruited as the experimental subjects. Volunteers were nonsmoking healthy individuals. Myopes with greater than 4 D were excluded. Volunteers were also excluded if they used routine medications that might affect IOP.⁷ Experimental subjects included 15 Whites, 2 Asian or Pacific Islanders, 2 Hispanics, and 2 Native Americans. Informed consent was obtained after explanation of the nature and possible consequences of the study. There were 5 men and 16 women. Eleven female subjects used medication for estrogen replacement therapy. Other routine medications used by a single subject were hydroxyzine, lithium, nifedipine, and venlafaxine and, by 2 subjects, fluoxetine.

Experimental subjects underwent a complete ophthalmic examination showing absence of any eye disease. None of the subjects presented a narrow iridocorneal angle under slit-lamp examination. Normal visual field was verified using the Humphrey Field Analyzer (San Leandro, CA) with a full-threshold 24-2 examination. A normal visual field was determined by clinical review and by Statpac II criteria for abnormality. The mean deviation and corrected pattern SD were both within the 95% age-specific norm, and the Glaucoma Hemifield was within the 99% age-specific norm. Reliability of field data was evaluated using a 33% cutoff for false positive, false negative, and fixation loss. Measured by the Goldmann tonometer during office hours, sitting IOP levels of these subjects were in the range of 10 to 19 mm Hg (14.4 ± 2.6 mm Hg; mean ± SD).

Subjects were selected for having regular daily sleep of approximately 8 hours. Before the laboratory session, they were instructed to maintain an accustomed 8-hour sleep period (lights off) for 7 days. Subjects wore a wrist device (Actigraph; Ambulatory Monitoring, Ardsley, NY) to monitor physical activity and kept a wake/sleep log. Daily wake–sleep (light–dark) synchronization was enhanced by attention to regular patterns. They were told to abstain from alcohol and caffeine consumption for 3 days before the laboratory session.

Laboratory light-dark conditions were strictly controlled. Light intensity in each subject’s room was maintained at 500 to 1000 lux at eye level when standing. The 8-hour period of darkness in each subject’s room was adjusted to correspond to that subject’s accustomed sleep period. Clock times for the IOP measurements were also individualized to coordinate this period of darkness. However, relative measurement times were transformed to analyze results as if each subject slept from 11 PM to 7 AM.

Measurements of IOP were performed by experienced researchers using a pneumatonometer (model 30 Classic, Mentor O&O, Norwell, MA). One or two drops of 0.5% proparacaine were used as local anesthetic. Measurements were taken every 2 hours in each eye (12 times within 24 hours). A hard-copy printout was produced for each IOP measurement. Tonograph in the printout was visually inspected. The IOP value was accepted if the tonograph pattern was normal and the SD of IOP was less than 1 mm Hg. In unaccepted cases (<10%), another IOP measurement was taken. However, no more than 3 measurements were allowed. Among the repeated measurements, the IOP value with the least SD was selected.⁶ Subjects were awakened in the dark period, when necessary, and IOP was measured in near-total darkness. Researchers were equipped with infrared night vision goggles (AN/PVS-7B Dark Invader; Meyers, Redmond, WA) to aid dark period measurements. If subjects were awakened, IOP measurement was taken within 2 to 3 minutes. Subjects’ light exposure and sleep disturbance were kept to a minimum during the nocturnal IOP measurements. Room activities were continuously videotaped for 24 hours by infrared cameras.

Times for reporting to the laboratory were staggered between 9 AM and 9 PM (3 subjects every 2 hours) to minimize potential confounding of the order of repeated measurements with the 24-hour IOP pattern. Subjects stayed in the laboratory for the entire recording session of approximately 24 hours. In the light/wake period, measurements of IOP were taken first approximately 30 minutes after arriving and then every 2 hours. To separate postural and circadian factors, the subject was instructed to lie down in bed for 5 minutes before the bilateral IOP measurements in the supine position. Then, the subject sat for 5 minutes before the sitting IOP measurements. Subjects went to bed according to their scheduled lights-off times, and sleep was encouraged. Measurements of IOP in the dark period were taken only in the supine posture, at 30 minutes after lights-off and then 3 more times, each separated by 2 hours. Lights were turned back on after 8 hours of darkness, and subjects were awakened, if necessary. Intraocular pressure was measured 30 minutes later and every 2 hours thereafter.

Values of IOP from both eyes were averaged, and this average was used for data entry. Two data analysis approaches were used. First, mean values of IOP from the 21 subjects were calculated at each time point. The trough and the peak among these IOP means were determined. Averages of IOP data from the light/wake period (7 AM to 11 PM), the dark period (11 PM to 7 AM), the time block of 7 AM to 3 PM, and the time block of 3 to 11 PM were calculated. Statistical comparisons of IOP were made between the trough and the peak and between the light/wake and dark periods, using paired t-tests. Repeated-measures ANOVA with post-hoc Bonferroni tests⁸ was used to compare the averages of supine IOP data from the three time blocks (7 AM to 3 PM, 3 to 11 PM, and 11 PM to 7 AM). P < 0.05 was the criterion of significance.

Specific analyses were performed to evaluate the 24-hour rhythm of IOP. Based on the assumption that the 24-hour IOP rhythm resembled a cosine profile, the best-fitting cosine curve^{9 10} for the 12 IOP means was determined for each individual. Each best-fitting curve had a fitted peak, the acrophase, and the time of which represented the phase-timing of the rhythm. Also, the height of the fitted cosine curve (its amplitude) estimated the magnitude of the 24-hour rhythm. The null hypothesis of a random distribution of acrophases around the clock was evaluated statistically using the Rayleigh test.¹¹ Lack of a significance with the Rayleigh test would indicate that the 24-hour rhythms were not consistent in timing among subjects, whereas the alternative hypothesis would be that 24-hour rhythms exist with synchronized timing for the group.

	Results

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Data were first analyzed considering the habitual body postures (i.e., sitting during the day and supine at night). The 24-hour profile of the mean IOP for all 21 subjects is presented in Figure 1 . The lowest IOP occurred at the last measurement in the light/wake period (9:30 PM), and the highest IOP appeared at the first measurement in the dark period (11:30 PM). The difference between the trough and the peak was 8.6 ± 0.8 mm Hg (mean ± SEM, n = 21; P < 0.001, paired t-test). The mean supine IOP in the dark period, 23.1 ± 0.7 mm Hg, was significantly higher (P < 0.001, paired t-test) than the mean sitting IOP in the light/wake period (16.9 ± 0.5 mm Hg). The four IOP mean values in the dark period were relatively close to each other, and a sharp reduction occurred around the lights-on transition (7 AM). During the light/wake period, mean IOP was high in the early morning and continuously decreased toward the end of the light/wake period.

View larger version (26K): [in this window] [in a new window]   Figure 1. A comparison of 24-hour patterns of IOPs in the aging and the young volunteers. Solid symbols represent a group of 50- to 69-year-old volunteers (n = 21). Intraocular pressure was measured by a pneumatonometer 30 minutes after the odd hours in both the sitting (•) and the supine () positions during the light/wake period (7 AM–11 PM) and only in the supine position during the dark period (11 PM–7 AM). Error bars represent SEM. Previously published results6 from two separate groups of 18- to 25-year-old volunteers were included for comparison. In one group (n = 12), IOP was measured in the sitting position () during the light/wake period and in the other group (n = 21) in the supine position (). During the dark period, all measurements of IOP were performed with subjects supine. Participants started 24-hour experiments at different times evenly distributed in the light/wake period.

View larger version (33K): [in this window] [in a new window]   Figure 2. The estimates of the 24-hour rhythms of IOP in habitual positions are shown in polar coordinates. Least-square cosine-fitting technique was used for the estimation. The clock time of acrophase (fitted peak) is shown with the amplitude (height of the fitted curve) in the radial scale (mm Hg). Measurements of IOP were taken with subjects in the sitting position during the light/wake period (7 AM–11 PM) and in the supine position during the dark period (11 PM–7 AM). •, 21 aging volunteers (50–69 years of age); , 12 younger volunteers (18–25 years of age).6

Cosine fits of the 24-hour supine IOP data showed that 19 of 21 acrophases appeared between 1 AM and 3 PM (Fig. 3 ; solid triangles), and the mean acrophase was at 8 AM (±1.17 hour). Once postural influences were removed these acrophases were more dispersed than those in Figure 2 . The Rayleigh test did not reject the null hypothesis of a random circular distribution of acrophases (0.1 > P > 0.05). This indicated that there was no significant 24-hour IOP rhythm of cosine shape when only the supine IOP data were considered. The mean amplitude of these cosine fits was 2.1 ± 0.3 mm Hg.

View larger version (33K): [in this window] [in a new window]   Figure 3. The estimated 24-hour rhythms of IOP in the supine position are shown in polar coordinates. These rhythms are independent from the influence of body positions. , 21 aging volunteers (50–69 years of age); , 21 younger volunteers (18–25 years of age).6

	Discussion

Top Abstract Introduction Methods Results Discussion References

Intraocular structures, such as retinal ganglion cells, are under continuous influence of IOP throughout the day and night. Among the numerous factors that can affect IOP for various lengths of time, body posture is one of the most important factors.¹² We observed a consistent 24-hour IOP pattern in this sample of the aging population when sitting IOP in the day and supine IOP at night were considered. This 24-hour IOP pattern was generally similar to that in the young adults (Fig. 1) . Both age groups had low sitting IOPs in the light/wake period and higher supine IOPs in the dark period. A nocturnal IOP elevation in the elderly, measured also in habitual positions, was observed in a previous study.⁵

The substantial IOP difference between the sitting and supine postures observed during the light/wake period suggests that a significant portion of the nocturnal IOP elevation in these aging volunteers was due to the change of body position. A recumbent body position at night causes multiple hydrostatic changes in the body, including a redistribution of body fluid in the eye^{13 14 15} and an elevation of episcleral venous pressure.¹² A combination of these changes contributes to a consistent IOP elevation in the dark/sleep period compared with daytime upright posture.

One well-known physiological adjustment during the dark/sleep period in the eye is the slowdown of aqueous humor flow. It has been shown that change of body position has a limited effect on aqueous flow.¹⁶ The rate of aqueous flow during the dark/sleep period is about half that during the light/wake period in healthy adults.¹⁷ Such a significant nocturnal slowdown of aqueous flow would theoretically decrease IOP if other parameters of aqueous humor dynamics (outflow facility and episcleral venous pressure) in the Goldmann equation remain constant. Our results suggest that the nocturnal slowdown of aqueous flow per se is not sufficient to counterbalance the elevation of IOP caused by the postural change and possible circadian mechanisms.

Based on the cosine-fitting technique and the statistical analysis of circular distribution of acrophases, a posture-independent 24-hour IOP rhythm was not detected in these aging volunteers. However, an almost-significant trend (P < 0.1), with the mean cosine amplitude similar to that of our younger sample, was observed. In addition, a significant elevation of supine IOP between the late light/wake period and the early dark period was evident in Figure 1 and in a previous report.³ Therefore, the question of a posture-independent 24-hour IOP rhythm in the elderly needs further evaluation. Twenty four–hour variations in the supine IOP could result from residual effects of prior posture, from "masking" effects of darkness, sleep, or arousal from sleep, or from endogenous circadian mechanisms. To distinguish these factors, studies using constant recumbent posture, sleep deprivation, and a constant light condition might prove useful.

Because of a large increase in the supine IOP between 9:30 and 11:30 PM, the mean IOP was at the highest level at 30 minutes into the dark period. A sharp increase of supine IOP at the beginning of the dark period was not observed in our previous study with young adults (Fig. 1) . The physiological basis for the sharp IOP elevation at the beginning of the dark period is not known. It is possible that pupillary dilation in the darkness contributes to this elevation of supine IOP in the aging volunteers. The IOP elevation was not due to repeated samplings of a narrow iridocorneal angle, because none of the volunteers appeared to have an occludable angle. Perhaps, the earlier IOP peak in the dark period simply reflects a phase-advanced physiological parameter related to IOP. In the aging process, there are phase advances in several physiological parameters, such as body temperature and rapid eye movement.¹⁸

The mean acrophases for the aging and the younger volunteers were very close, as shown in Figure 2 (around 4 AM) and Figure 3 (around 8 AM). However, individual 24-hour IOP patterns in the aging population were more variable, which is evident from the more dispersed acrophases in Figures 2 and 3 . The mean amplitudes and the standard deviations in Figure 2 were also similar in the young and elderly (data not shown). When examining the supine IOP data of the aging volunteers (Fig. 3) , the SD in the amplitude was larger than that of the younger volunteers (with a similar mean). Therefore, clock timing and amplitude of the posture-independent IOP change are more variable in the aging volunteers than in the younger volunteers. In the aging process, many hormones modulate their secretions and circulating levels around the circadian clock.¹⁹ Although which hormones are related to the posture-independent IOP elevation at night is unclear, two hormones that have increased plasma concentrations at night deserve mention. One is cortisol, which shows a phase-advance during sleep in the elderly.²⁰ It is well known that glucocorticoid may increase IOP after a systemic or topical application. Another hormone is melatonin, which has a more dispersed 24-hour pattern in the aging population.²¹ However, orally administered melatonin is reported to cause a decrease in human IOP.²²

Our data showed that the mean IOP in this aging sample was slightly higher than the mean IOP in the younger volunteers throughout the 24 hours. This agrees with the generally accepted notion that IOP in the elderly is higher than that in the young adult,²³ at least during the light/wake period, although neither the present aging sample nor the younger sample⁶ has been proved to be a representative of the general population. The individuals selected for this study are probably healthier and more drug-free than the average person in the aging population. It should be noted that 6 experimental subjects in our aging sample used a medication routinely to control anxiety (hydroxyzine), blood pressure (nifepidine), or depression (lithium, venlafaxine, and fluoxetine in 2 cases). These medications may have unknown or minor effects on the level of IOP.

After the habitual change of body position from upright to recumbent at night, redistribution of more blood to the eye may not be the only effect on nocturnal ocular perfusion in the elderly. The nocturnal elevation of IOP coincides with the time when brachial blood pressure is low,²⁴ so the elevated IOP may lead to a decrease in ocular perfusion pressure at night. There would be fine adjustments of ocular blood flow under the influences of posture, systemic and local blood pressures, and age.²⁵ Additional adjustments along the circadian clock by unknown physiological factors may also be critical. If reduced blood perfusion in the eye contributes to the pathogenesis of glaucoma, investigations of ocular blood flow in the elderly, at night and in the supine position, may improve our understanding of the significance of aging as another important risk factor for glaucoma.

	Acknowledgements

 
The authors thank Judy M. Nisbet for her excellent technical assistance.

	Footnotes

 
Supported by NIH Grant EY07544 and the Sam and Rose Stein Institute for Research on Aging.

Submitted for publication January 26, 1999; revised May 27, 1999; accepted July 14, 1999.

Commercial relationships policy: N.

Corresponding author: John Liu, University of California, San Diego, Department of Ophthalmology, La Jolla, CA 92093-0946. E-mail: joliu{at}ucsd.edu

	References

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