April 2012
Volume 53, Issue 4
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Multidisciplinary Ophthalmic Imaging  |   April 2012
Circadian Changes in Subfoveal Choroidal Thickness and the Relationship with Circulatory Factors in Healthy Subjects
Author Affiliations & Notes
  • Shinichi Usui
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Yasushi Ikuno
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Masahiro Akiba
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Ichiro Maruko
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Tetsuju Sekiryu
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Kohji Nishida
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Tomohiro Iida
    From the National Hospital Organization, Osaka National Hospital, Osaka, Japan; Department of Ophthalmology, Osaka University Graduate School of Medicine, Osaka, Japan; Choroidal Imaging Group; Topcon Corporation, Tokyo, Japan; Department of Ophthalmology, Fukushima Medical University School of Medicine, Fukushima, Japan.
  • Corresponding author: Yasushi Ikuno, Department of Ophthalmology E7, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan; ikuno@ophthal.med.osaka-u.ac.jp
Investigative Ophthalmology & Visual Science April 2012, Vol.53, 2300-2307. doi:10.1167/iovs.11-8383
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      Shinichi Usui, Yasushi Ikuno, Masahiro Akiba, Ichiro Maruko, Tetsuju Sekiryu, Kohji Nishida, Tomohiro Iida; Circadian Changes in Subfoveal Choroidal Thickness and the Relationship with Circulatory Factors in Healthy Subjects. Invest. Ophthalmol. Vis. Sci. 2012;53(4):2300-2307. doi: 10.1167/iovs.11-8383.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose: To investigate circadian changes in subfoveal choroidal thickness (SFCT) and the relation to systemic factors in healthy subjects.

Methods: Thirty-eight eyes of 19 healthy volunteers were enrolled. SFCT was measured by using prototype high-penetration optical coherence tomography. Intraocular pressure (IOP), systolic blood pressure (SBP), diastolic blood pressures (DBP), and heart rate (HR) were measured every 3 hours over a 24-hour period. Circadian changes in the mean arterial pressure (MAP) and mean ocular perfusion pressure (MOPP) were calculated. The difference between the maximal and minimal SFCTs was analyzed, and correlations between the SFCT and other systemic factors were evaluated.

Results: There was a significant circadian variation in SFCT (P < 0.0001). The total mean SFCT was 280.3 ± 106.1 μm. At 6 PM, the mean SFCT (271.9 ± 103.5 μm) was the thinnest and at 3 AM it was the thickest (290.8 ± 110.8 μm). The SFCTs in 32 of 38 eyes were thickest between 3 and 9 AM and in 27 of 38 eyes, thinnest between 3 and 9 PM. The mean SFCT was significantly negatively correlated with the mean SBP (R2 = 0.59, P = 0.02) in all eyes. There were no significant correlations between the mean SFCT and the mean DBP, MAP, HR, IOP, and MOPP in all eyes.

Conclusions: We investigated the circadian change of choroidal thickness using high-penetration optical coherence tomography in healthy volunteers. The significant diurnal change was found and the choroid was thicker at night and thinner in daytime. Fluctuations in the choroidal thickness may be related to SBP.

Introduction
Investigators are increasingly interested in choroidal imaging using optical coherence tomography (OCT). The choroidal thickness can be measured with commercially available OCT instruments by using the enhanced depth-imaging (EDI) technique 1 or high-penetration OCT with a longer wavelength. 27 The EDI technique is based on 50 to 100 averaged scans of the flipped B-scan images, which raises the signal-to-noise ratio and as a result, provides images of the deep posterior tissues. High-penetration OCT is based on a longer-wavelength light source, which allows higher penetration at the retinal pigment epithelium (RPE). Both systems provide images of the full-thickness choroid, which enables one to obtain the choroidal thickness that normally is represented by the distance between the RPE and the chorioscleral interface. Manual measurements of the choroidal thickness are highly reliable and reproducible despite higher interindividual variations in the choroidal structure. 8 Observing the choroid by using these OCT techniques is useful for studying the morphologic changes associated with many choroidal disorders, such as high myopia–related chorioretinal atrophies, 9,10 central serous chorioretinopathy (CSC), 11 age-related macular degeneration, 12,13 polypoidal choroidal vasculopathy, 1214 and Vogt-Koyanagi-Harada disease. 15  
Photodynamic therapy reduces the choroidal thickness in CSC. 11 The choroid, a fully vascularized structure, is supplied by the posterior ciliary arteries, which branch from the ophthalmic artery and account for 85% of the total ocular blood flow. 16,17 Choroidal vessels are poorly autoregulated and changes in perfusion pressure directly affect the blood flow. 1820 Choroidal thickness has a diurnal rhythm in some species such as chickens 21 and marmosets. 22 The presence of diurnal fluctuations in human choroidal thickness also has been suggested by findings obtained throughout a 12-hour period with a signal-processing technique, 23,24 but this is still uncertain. In the current study, changes in subfoveal choroidal thickness (SFCT) were measured over a 24-hour period by using high-penetration OCT with a 1050-nm wavelength light source, and the relation to systemic factors was evaluated in healthy adults. 
Methods
Subjects
Thirty-eight eyes of 19 healthy volunteers with no ophthalmic or systemic symptoms were enrolled. Exclusion criteria included the presence of any macular abnormalities such as choroidal neovascularization, asymptomatic pigment epithelial detachment, or whitish myopic atrophy; any systemic abnormalities under treatment such as vascular disease, hypertension, and diabetes mellitus; and a history of intraocular surgery. 
SFCT, intraocular pressure (IOP), systolic blood pressure (SBP), diastolic blood pressure (DBP), and heart rate (HR) were measured every 3 hours over a 24-hour period from 3 PM to noon of the following day, and diurnal changes in the mean arterial pressure (MAP) and mean ocular perfusion pressure (MOPP) were calculated according to the following formulas: MAP = DBP + ⅓(SBP − DBP) and MOPP = ⅔(MAP − IOP). The refractive error (RE), axial length (AL), and central corneal thickness (CCT) were measured at baseline (2 PM). All of the examinations were performed in sitting position. Each experimental session was completed within 30 minutes. Artificial light was turned off at 10 PM and on at 6 AM. Subjects slept in the upright position between 10 PM and 6 AM except at midnight and 3 AM when they were awoken for measurements. 
The institutional review board of Osaka University Hospital approved use of the prototype high-penetration OCT and this observational study. The research adhered to the tenets of the Declaration of Helsinki. 
Prototype High-Penetration OCT
The prototype high-penetration OCT (swept-source OCT; Topcon, Tokyo, Japan) was used to image the full-thickness choroid. This OCT instrument is based on a swept-source technology with a scan speed of 100,000 A-scans per second. The center wavelength of the light beam is 1050 nm. This wavelength has improved ability for penetrating deeper tissue through the RPE into the choroid. The sweeping bandwidth of the light source is approximately 100 μm centered around 1050 nm; however, the effective bandwidth is reduced to approximately 60 to 70 nm owing to water absorption of the eye and the windowing function in the signal processing. Effective axial resolution was 8 μm in tissue. Note that the axial resolution may degrade with depth but that degradation will be slight. Choroidal thickness was defined as the distance between the hyperscattering line of the RPE and that of the chorioscleral interface. 8 Three masked clinicians measured SFCT every 3 hours by using a built-in caliper function in OCT viewer software. Thirty-two single B-scan images were averaged to have better visualization of choroid and sclera. 
Other Examinations
RE and corneal refraction were measured by autorefractometry (ARK-700A; Nidek, Gamagori, Japan). The AL was measured by partial optical coherence inferometry (IOLMaster; Carl Zeiss Meditec, La Jolla, CA). CCT was measured by specular microscopy (AP3000P; Topcon). IOP was measured with a handheld tonometry device (Icare; Tiolat Oy, Helsinki, Finland). SBP, DBP, and HR were measured by automatic sphygmomanometer (CH-483C; Citizen, Tokyo, Japan). 
Statistical Analysis
The data were analyzed by using a repeated-measures analysis of variance for fluctuation of SFCT. Correlations between mean level of SFCT and mean level of the other systemic factors were evaluated by Pearson's correlation coefficient and multiple stepwise regression analysis by using statistical software (JMP 8.0; SAS Inc., Cary, NC). P < 0.05 was considered significant. 
Results
Demographic Data
The demographic data are shown in Table 1. Ten men and nine women (mean age, 34.8 ± 8.6 years; range, 22–51 years) participated in the study. Most subjects were myopic. The mean RE was −4.4 ± 2.4 diopters (D) (range, −8.25 to 1.375 D), and the mean AL was 25.4 ± 1.0 mm (range, 22.94–27.35 mm). The corneal parameters were within the normal range; the mean CCT was 0.513 ± 0.031 mm (range, 0.447–0.558 mm); and the mean corneal refraction was 43.2 ± 1.4 D (range, 40.25–46.25 D). 
Table 1.
 
Demographic Data
Table 1.
 
Demographic Data
Parameters Mean ± SD
Age, y 34.8 ± 8.6
RE, D −4.4 ± 2.4
AL, mm 25.4 ± 1.0
CCT, mm 0.513 ± 0.031
Corneal refraction, D 43.2 ± 1.4
Circadian Changes in SFCT
Fig. 1 shows a typical image from high-penetration OCT. The RPE and chorioscleral interface were clearly identified in all cases. Circadian changes in the mean SFCT from 38 eyes of 19 subjects are shown in Fig. 2A and Table 2. SFCT became thinner during the day and thicker at night. The mean all SFCT was 280.3 ± 106.1 μm. Overall, the mean SFCT was thinnest at 6 PM (mean, 271.9 ± 103.5 μm) and thickest at 3 AM (mean, 290.8 ± 110.8 μm). Right eye and left eye had a different peak time; however, the trend of day/night cycle was quite similar (daytime low and nighttime high). The mean SFCT from 19 subjects had a wide standard deviation because SFCTs varied widely among subjects. Therefore, the points at which SFCTs were the thinnest and thickest in each subject (Table 3) were evaluated. The SFCTs in 32 of 38 eyes were thickest between 3 and 9 AM, and in 27 of 38 eyes, thinnest between 3 and 9 PM (Fig. 2B). Moreover, the amplitudes of diurnal fluctuations in SFCTs differed among the subjects (Fig. 2C). The largest fluctuation in SFCT was 65 μm; the smallest fluctuation was 8 μm. A repeated-measures analysis of variance showed a highly significant difference between the maximal and minimal SFCTs (P < 0.0001, within-subjects time of effect); the average mean diurnal fluctuation of SFCT was about 33 μm (Table 4). This was also shown in the analysis of the right eye and left eye independently (P < 0.0001 for the right and P < 0.0001 for the left, within-subjects time of effect). 
Figure 1.
 
Representative image of high-penetration OCT. The image clearly shows the entire retina and choroid. The choroidal thickness is defined as the distance from the RPE to the chorioscleral interface.
Figure 1.
 
Representative image of high-penetration OCT. The image clearly shows the entire retina and choroid. The choroidal thickness is defined as the distance from the RPE to the chorioscleral interface.
Figure 2.
 
Circadian changes in SFCT. (A) The circadian changes in the mean SFCT measured every 3 hours over a 24-hour period. The mean SFCTs increased at night and decreased during the day. The mean SFCT of all eyes at 6 PM was the thinnest (271.9 ± 103.5 μm) and that at 3 AM was the thickest (290.8 ± 110.8 μm). The trend of day/night cycle of the right eye and left eye was quite similar. (B) The number of eyes at each time point during which the minimal and maximal SFCTs are seen. The minimal SFCT was seen between 3 and 9 PM, and the maximal SFCT was seen between 3 and 9 AM in most eyes. (C) Individual diurnal fluctuations in SFCT. The amplitudes of the maximal minus the minimal SFCTs are shown for all subjects. A variation in circadian fluctuations in SFCT was found. The largest fluctuation in SFCT was 65 μm in the left eye of subject 1, and the smallest fluctuation in SFCT was 8 μm in the left eye of subject 10. R, right eye; L, left eye.
Figure 2.
 
Circadian changes in SFCT. (A) The circadian changes in the mean SFCT measured every 3 hours over a 24-hour period. The mean SFCTs increased at night and decreased during the day. The mean SFCT of all eyes at 6 PM was the thinnest (271.9 ± 103.5 μm) and that at 3 AM was the thickest (290.8 ± 110.8 μm). The trend of day/night cycle of the right eye and left eye was quite similar. (B) The number of eyes at each time point during which the minimal and maximal SFCTs are seen. The minimal SFCT was seen between 3 and 9 PM, and the maximal SFCT was seen between 3 and 9 AM in most eyes. (C) Individual diurnal fluctuations in SFCT. The amplitudes of the maximal minus the minimal SFCTs are shown for all subjects. A variation in circadian fluctuations in SFCT was found. The largest fluctuation in SFCT was 65 μm in the left eye of subject 1, and the smallest fluctuation in SFCT was 8 μm in the left eye of subject 10. R, right eye; L, left eye.
Table 2.
 
Circadian Changes in Subfoveal Choroidal Thickness
Table 2.
 
Circadian Changes in Subfoveal Choroidal Thickness
SFCT (Mean ± SD) Average 3 PM 6 PM 9 PM Midnight 3 AM 6 AM 9 AM Noon
Right eye, μm 280.8 ± 103.5 272.6 ± 106.6 274.3 ± 102.3 274.4 ± 105.0 280.3 ± 101.1 290.7 ± 108.7 292.1 ± 106.7 282.0 ± 99.9 280.2 ± 100.9
Left eye, μm 279.8 ± 111.4 277.2 ± 110.3 269.5 ± 107.4 274.2 ± 110.4 277.4 ± 111.0 290.9 ± 115.8 286.9 ± 117.8 282.6 ± 112.2 279.5 ± 109.7
All eyes, μm 280.3 ± 106.1 274.9 ± 107.0 271.9 ± 103.5 274.3 ± 106.2 278.9 ± 104.7 290.8 ± 110.8 289.5 ± 110.9 282.3 ± 104.8 279.9 ± 103.9
Table 3.
 
Ocular Biometric Parameters and Fluctuations of Subfoveal Choroidal Thickness for Each Subject
Table 3.
 
Ocular Biometric Parameters and Fluctuations of Subfoveal Choroidal Thickness for Each Subject
Subject Age (y) Sex Eye RE (D) AL (mm) CCT (mm) Corneal Refraction (D) Total Mean S FCT (μm) (Mean ± SD) Min SFCT (μm/Time) Max SFCT (μm/Time) (Max − Min) SFCT (μm)
 1 37 M R −5.375 26.35 0.539 43 410.3 ± 17.6 384/6 PM 441/6 AM 57
L −4.875 26.19 0.542 42.75 398.8 ± 23.0 366/9 PM 431/3 AM 65
 2 31 M R −4.375 24.83 0.542 44.75 227.0 ± 5.96 218/Midnight 235/6 AM 17
L −3.25 24.07 0.54 44.75 304.8 ± 6.2 296/6 PM 315/3 AM 19
 3 28 M R −0.625 24.39 0.518 40.75 308.7 ± 11.3 284/9 PM 320/3 PM 36
L −0.125 24.27 0.521 40.75 324.2 ± 14.8 292/9 PM 337/9 AM 45
 4 44 M R −3.625 26.25 0.547 41.25 287.0 ± 7.9 276/9 PM 296/3 AM 20
L −4.625 26.78 0.543 41 168.8 ± 11.1 150/6 PM 182/6 AM 32
 5 39 M R −7.375 25.99 0.447 43.75 284.0 ± 13.6 259/3 PM 305/6 AM 46
L −7.375 25.99 0.447 43.5 289.2 ± 7.7 281/6 AM 300/6 PM 19
 6 28 F R −3.5 25.02 0.483 43.25 316.6 ± 9.2 299/Midnight 329/3 AM 30
L −5 25.65 0.478 43.25 241.5 ± 8.2 229/6 PM 252/3 AM 23
 7 29 F R −6.5 26.3 0.476 43.25 199.1 ± 16.5 169/6 PM 217/6 AM 48
L −6.25 26.2 0.483 43.25 196.8 ± 17.8 173/6 PM 225/3 AM 52
 8 38 M R −3.875 25.72 0.548 43.25 238.2 ± 17.2 199/3 PM 258/6 AM 58
L −4.25 26.05 0.55 43.25 221.5 ± 9.8 199/3 AM 231/9 PM 32
 9 50 M R −7.875 27.35 0.548 43.25 169.8 ± 8.6 159/3 PM 185/3 AM 26
L −7.25 26.72 0.536 43.25 179.7 ± 15.7 162/9 PM 209/3 AM 37
10 51 M R −2.75 26.42 0.493 40.5 164.0 ± 4.41 156/9 PM 167/9 AM 11
L −2.125 25.94 0.5 40.25 197.9 ± 5.2 188/9 PM 296/6 PM 8
11 27 M R −6.875 25.32 0.52 46.25 359.0 ± 7.71 347/6 PM 371/3 AM 24
L −5.5 25.16 0.53 46 354.2 ± 13.7 331/6 PM 379/6 AM 48
12 24 F R −4.125 25.37 0.552 43 258.7 ± 10.6 246/6 PM 275/6 AM 29
L −3.75 25.18 0.543 43.25 314.8 ± 10.4 304/6 PM 331/6 AM 27
13 27 F R −0.625 23.9 0.507 42.25 434.1 ± 17.7 412/Noon 449/6 AM 37
L −0.625 24.05 0.516 41.75 462.4 ± 19.5 436/6 PM 492/3 AM 56
14 36 F R −6 25.02 0.558 45 149.2 ± 11.7 136/9 PM 164/Midnight 28
L −5.75 24.58 0.555 45.25 115.1 ± 3.6 110/6 PM 119/3 AM 9
15 22 M R −5.75 25.28 0.521 44 285.1 ± 11.2 274/3 PM 308/3 AM 34
L −7.875 25.84 0.513 44.5 286.2 ± 7.84 272/6 PM 296/6 AM 24
16 47 F R 1.375 22.94 0.47 42.75 544.6 ± 14.9 523/9 AM 562/6 AM 39
L 0.75 23.18 0.475 42.75 557.8 ± 13.0 547/6 PM 584/6 AM 37
17 38 F R −3.625 25.38 0.475 42.5 326.0 ± 15.5 306/9 PM 351/3 AM 45
L −4.25 25.59 0.488 42.5 334.4 ± 14.4 319/Midnight 357/3 AM 38
18 37 F R −8.25 26.71 0.516 44.5 177.8 ± 8.0 167/9 AM 190/6 AM 23
L −6 26.03 0.503 44 180.4 ± 6.5 168/Noon 189/Midnight 21
19 29 F R −6.25 24.96 0.502 44.75 196.8 ± 7.1 188/Noon 206/6 AM 18
L −5.625 24.84 0.495 44.5 187.2 ± 5.8 183/6 AM 198/3 AM 15
Table 4.
 
Amplitude of Fluctuations in Subfoveal Choroidal Thicknesses
Table 4.
 
Amplitude of Fluctuations in Subfoveal Choroidal Thicknesses
SFCT Max SFCT − Min SFCT (μm), Mean ± SD Range (μm), Mean ± SD P *
Right eye 33.0 ± 13.4 26.5 ± 10.1 to 39.5 ± 19.8 <0.0001
Left eye 33.0 ± 15.5 25.4 ± 11.7 to 40.5 ± 23.0 <0.0001
All eyes 33.0 ± 14.3 28.3 ± 11.7 to 37.7 ± 18.5 <0.0001
Circadian Changes in Systemic Factors and Relationship to SFCT
Circadian changes in the systemic factors are shown in Fig. 3. The mean SBP decreased during the night, that is, the trend was opposite to that of SFCT whose thickness increased during the night. In fact, SFCT was negatively correlated with SBP in all eyes (R 2 = 0.59, P = 0.02) (Table 5). The analysis of each eye (right/left) showed a significant correlation in the right (P = 0.02) and left (P = 0.04). The rhythms of DBP, MAP, HR, IOP, and MOPP in all eyes, however, did not coincide with the rhythm of SFCT (Fig. 3, Table 5). IOP decreased during the night but was not correlated with SFCT. SBP was the parameter that had the highest correlation with the fluctuation of SFCT among SBP, DBP, MAP, HR, IOP, MOPP with stepwise multiple regression analysis (Table 6). The value of its correlation coefficient was −2.04. Circadian change of SBP for each subject showed that SBPs in 16 of 19 subjects were highest between noon and 9 PM and in 14 of 19 subjects were lowest between midnight and 9 AM (Table 7). 
Figure 3.
 
Circadian changes in SBP, DBP, MAP, HR, IOP, and MOPP were measured every 3 hours throughout a 24-hour period. The SBP decreased at night, which is the opposite trend to that of the thickened choroid. The rhythms of DBP, MAP, and MOPP, which were high at 6 PM and low at 9 AM, were similar to each other. The DBP was also high at 3 AM. The HR was high at 9 PM and the IOP was high during the day and low at night.
Figure 3.
 
Circadian changes in SBP, DBP, MAP, HR, IOP, and MOPP were measured every 3 hours throughout a 24-hour period. The SBP decreased at night, which is the opposite trend to that of the thickened choroid. The rhythms of DBP, MAP, and MOPP, which were high at 6 PM and low at 9 AM, were similar to each other. The DBP was also high at 3 AM. The HR was high at 9 PM and the IOP was high during the day and low at night.
Table 5.
 
Relationship between Subfoveal Choroidal Thickness and Other Systemic Factors
Table 5.
 
Relationship between Subfoveal Choroidal Thickness and Other Systemic Factors
Factor Right Eye Left Eye All Eyes
Coefficient R2 P Value Coefficient R2 P Value Coefficient R2 P Value
SBP −0.27 0.59 0.02* −0.27 0.53 0.04* −0.28 0.59 0.02*
DBP 0.07 0.06 0.54 0.01 0.002 0.90 0.04 0.02 0.70
MAP −0.04 0.03 0.64 −0.08 0.11 0.40 −0.06 0.07 0.51
HR −0.22 0.56 0.03* −0.17 0.29 0.16 −0.21 0.44 0.06
IOP −0.02 0.02 0.70 <0.01 <0.01 0.99 −0.01 <0.01 0.85
MOPP −0.02 0.02 0.72 −0.05 0.11 0.40 −0.03 0.04 0.61
Table 6.
 
Stepwise Regression Analysis for Influential Factors on Choroidal Thickness of All Eyes
Table 6.
 
Stepwise Regression Analysis for Influential Factors on Choroidal Thickness of All Eyes
Factor P
SBP 0.025*
DBP 0.48
MAP 0.48
HR 0.35
IOP 0.49
MOPP 0.88
Table 7.
 
Circadian Change of Systolic Blood Pressure (mm Hg) for Each Subject
Table 7.
 
Circadian Change of Systolic Blood Pressure (mm Hg) for Each Subject
Subject 3 PM 6 PM 9 PM Midnight 3 AM 6 AM 9 AM Noon
 1 127 130* 118 127 127 113† 116 126
 2 109 128* 118 108 120 128* 110 102†
 3 121* 116 114 113 112 104† 104† 110
 4 126 135* 115† 126 119 121 132 130
 5 117 122 125* 115 110† 122 116 122
 6 112* 106 109 100† 100† 107 102 107
 7 120* 113 117 113 110 104† 110 107
 8 109† 123 128* 112 109† 118 116 115
 9 136* 130 122 128 114† 123 116 134
10 181* 165 173 167 154 145† 173 180
11 113 112 115* 109 114 115* 96† 110
12 109 107† 120 115 128* 116 115 117
13 106* 96 104 92† 100 103 106* 101
14 114* 112 95† 110 109 100 99 110
15 126 115 119 103† 126 115 116 134*
16 119† 123 136 137* 130 120 123 135
17 107* 97 95 92† 94 95 94 100
18 115 118 113 120* 102 112 99† 107
19 104 121* 102 104 100† 105 100† 102
Discussion
The authors measured the choroidal thickness over a 24-hour period by using high-penetration OCT and found that the SFCT in humans increased during the night and decreased during the day. Recently, Chakraborty et al. 24 have reported the findings of a large study to investigate the diurnal variations in 30 healthy eyes and have shown that the choroid is thickest at night and thinnest in the morning by using a signal-processing technique throughout a 12-hour period over two consecutive days. They have also monitored AL and IOP and found a negative correlation between choroidal thickness and AL. 24 The current study supported this result by carrying out measurements across a full 24-hour period and by measuring the choroid with high-penetration OCT. The finding of choroidal-thickness diurnal changes (thicker at night and thinner at daytime) is in agreement with 2 previous reports. 23,24 Brown and associates 23 have found a similar trend with a mean maximum–minimum difference of 59.4 μm. Chakraborty and associates 24 have reported the mean amplitude as 29 μm. The current study showed a mean amplitude of 33.0 μm in overall eyes (33.0 μm in the right and 33.0 μm in the left), which is in agreement with that study. 
The fluctuation of choroidal thickness was also similar to that in normal chickens 21 and marmosets. 22 A previous report has suggested that changes in choroidal thickness are related to fluctuations in AL and IOP in chickens, 21 that is, the choroid becomes thicker during the night when the eye is shortest and thinner during the day when the eye is longest. 21 The phases of the rhythm in AL generally coincide with the rhythm of IOP, which is high during the day in chicks. 25 In humans, the rhythm of IOP is similar to that of chicks, that is, high during the day and low during the night. 26 The diurnal fluctuations in the mean IOP in the current study were almost the same as those reported previously. Chakraborty et al. 24 have reported a positive association between AL and IOP. However, it is difficult to explain the mechanism of choroidal and AL fluctuations, based only on IOP fluctuations. In this study, the authors did not find a correlation between fluctuations in IOP and choroidal thickness. IOP may be one factor responsible for diurnal fluctuations in the choroidal thickness and AL. Several reports have supported the finding that IOP is not the only factor that affects AL. 22,27  
Retinal defocus and scleral stiffness also affect choroidal fluctuations. In chick eyes, the retina moves forward with myopic defocus and backward with hyperopic defocus with changes in the choroidal thickness and a compensatory response in emmetropization. 28 Furthermore, synthesis of extracellular matrix glycosaminoglycans in chick sclera exhibits a circadian rhythm that may affect the rhythm in axial elongation. 29  
The ocular blood flow is also an important factor explaining the mechanism of SFCT fluctuations, because choroidal blood flow is poorly autoregulated. The authors evaluated the relationship between choroidal thickness and some circulatory factors and found a relationship in the diurnal rhythm between the SBP, which decreased at night, and choroidal thickness, which increased at night. There are several reports about the relationship between choroidal blood flow and other factors. Straubhaar et al. 30 have demonstrated that MAP has no influence on the choroidal laser doppler flowmetry parameters, whereas choroidal volume increases significantly with increased IOP. Riva et al. 31 have investigated the response of choroidal blood flow to increases in MOPP induced by isometric exercises and found that an increase in MOPP of up to 67% induces an increase in choroidal vascular resistance, which limits the increase in choroidal blood flow to approximately 12%. Polska et al. 32 have investigated choroidal blood flow regulation during combined changes in IOP and systemic arterial blood pressure and shown that the choroid had some autoregulatory capacity; moreover, choroidal blood flow depends not only on ocular perfusion pressure, but also on MAP and IOP. However, in the current study, the authors found only a correlation between SFCT and SBP, although other factors also may be correlated with SFCT, according to others' findings. There are some reports of the relationship between choroidal blood flow and systemic factors in diabetic patients. Choroidal blood flow appears to decrease in patients with severe diabetic retinopathy owing to increased vascular resistance and a decreased ocular perfusion pressure. 33 Pulsatile ocular blood flow appears to be higher in diabetics. 34 Presence of systemic hypertension may increase the choroidal blood flow in diabetic patients. 35  
Other investigators have reported abnormalities in the ocular circulation in patients with glaucoma. Loss of autoregulation in ocular blood flow may be present in primary open-angle glaucoma (POAG). 36,37 Several studies have reported blood flow disturbances including slower choroidal circulation, 38 low blood pressure, nocturnal hypotension, and fluctuations in MOPP in patients with normal tension glaucoma (NTG). 39 Pemp et al. 40 have reported that patients with POAG show a larger diurnal fluctuation of ocular blood flow. Fuchsjäger-Mayrl et al. 41 have shown reduced choroidal blood flow and an abnormal association between blood pressure and ocular perfusion in patients with POAG. Kochhorov et al. 42 have analyzed short-term variability of SBP and choroidal blood flow in glaucoma patients and found a higher short-term variability of both SBP and choroidal blood flow in POAG patients. However, our finding of the correlation between SBP and choroidal thickness in healthy subjects may be in keeping with the results of Kochhorov and colleagues; it is unclear whether the relation between these two parameters is dependent or independent. Recently, several groups have evaluated the relationship between choroidal thickness and glaucoma by using OCT. Mwanza et al. 43 have reported that the choroidal thickness does not differ among healthy subjects and patients with NTG and POAG. Maul et al. 44 have concluded that the degree of glaucomatous damage is not consistently associated with choroidal thickness; however, the authors 45 have recently reported choroidal thinning in young, highly myopic patients with NTG. Further studies are needed to clarify the relation between glaucoma and choroidal thickness because of the multifactorial pathogenesis of glaucoma. Future studies of choroidal thickness in glaucoma should incorporate an awareness of the potential of choroidal thickness to fluctuate diurnally; these changes should be taken into account to avoid confounding of results. 
In conclusion, the authors found circadian fluctuations in SFCT that may relate to SBP in healthy adults. Evaluating choroidal fluctuations in detail may be a key factor in assessing glaucoma and ocular growth. 
Acknowledgments
The authors thank Toshimitsu Hamasaki, PhD, Department of Biostatistics, Osaka University Medical School, for assistance in data analysis. 
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Footnotes
 Disclosure: S. Usui, None; Y. Ikuno, None; M. Akiba, Topcon Corporation (E); I. Maruko, None; T. Sekiryu, None; K. Nishida, None; T. Iida, None
Figure 1.
 
Representative image of high-penetration OCT. The image clearly shows the entire retina and choroid. The choroidal thickness is defined as the distance from the RPE to the chorioscleral interface.
Figure 1.
 
Representative image of high-penetration OCT. The image clearly shows the entire retina and choroid. The choroidal thickness is defined as the distance from the RPE to the chorioscleral interface.
Figure 2.
 
Circadian changes in SFCT. (A) The circadian changes in the mean SFCT measured every 3 hours over a 24-hour period. The mean SFCTs increased at night and decreased during the day. The mean SFCT of all eyes at 6 PM was the thinnest (271.9 ± 103.5 μm) and that at 3 AM was the thickest (290.8 ± 110.8 μm). The trend of day/night cycle of the right eye and left eye was quite similar. (B) The number of eyes at each time point during which the minimal and maximal SFCTs are seen. The minimal SFCT was seen between 3 and 9 PM, and the maximal SFCT was seen between 3 and 9 AM in most eyes. (C) Individual diurnal fluctuations in SFCT. The amplitudes of the maximal minus the minimal SFCTs are shown for all subjects. A variation in circadian fluctuations in SFCT was found. The largest fluctuation in SFCT was 65 μm in the left eye of subject 1, and the smallest fluctuation in SFCT was 8 μm in the left eye of subject 10. R, right eye; L, left eye.
Figure 2.
 
Circadian changes in SFCT. (A) The circadian changes in the mean SFCT measured every 3 hours over a 24-hour period. The mean SFCTs increased at night and decreased during the day. The mean SFCT of all eyes at 6 PM was the thinnest (271.9 ± 103.5 μm) and that at 3 AM was the thickest (290.8 ± 110.8 μm). The trend of day/night cycle of the right eye and left eye was quite similar. (B) The number of eyes at each time point during which the minimal and maximal SFCTs are seen. The minimal SFCT was seen between 3 and 9 PM, and the maximal SFCT was seen between 3 and 9 AM in most eyes. (C) Individual diurnal fluctuations in SFCT. The amplitudes of the maximal minus the minimal SFCTs are shown for all subjects. A variation in circadian fluctuations in SFCT was found. The largest fluctuation in SFCT was 65 μm in the left eye of subject 1, and the smallest fluctuation in SFCT was 8 μm in the left eye of subject 10. R, right eye; L, left eye.
Figure 3.
 
Circadian changes in SBP, DBP, MAP, HR, IOP, and MOPP were measured every 3 hours throughout a 24-hour period. The SBP decreased at night, which is the opposite trend to that of the thickened choroid. The rhythms of DBP, MAP, and MOPP, which were high at 6 PM and low at 9 AM, were similar to each other. The DBP was also high at 3 AM. The HR was high at 9 PM and the IOP was high during the day and low at night.
Figure 3.
 
Circadian changes in SBP, DBP, MAP, HR, IOP, and MOPP were measured every 3 hours throughout a 24-hour period. The SBP decreased at night, which is the opposite trend to that of the thickened choroid. The rhythms of DBP, MAP, and MOPP, which were high at 6 PM and low at 9 AM, were similar to each other. The DBP was also high at 3 AM. The HR was high at 9 PM and the IOP was high during the day and low at night.
Table 1.
 
Demographic Data
Table 1.
 
Demographic Data
Parameters Mean ± SD
Age, y 34.8 ± 8.6
RE, D −4.4 ± 2.4
AL, mm 25.4 ± 1.0
CCT, mm 0.513 ± 0.031
Corneal refraction, D 43.2 ± 1.4
Table 2.
 
Circadian Changes in Subfoveal Choroidal Thickness
Table 2.
 
Circadian Changes in Subfoveal Choroidal Thickness
SFCT (Mean ± SD) Average 3 PM 6 PM 9 PM Midnight 3 AM 6 AM 9 AM Noon
Right eye, μm 280.8 ± 103.5 272.6 ± 106.6 274.3 ± 102.3 274.4 ± 105.0 280.3 ± 101.1 290.7 ± 108.7 292.1 ± 106.7 282.0 ± 99.9 280.2 ± 100.9
Left eye, μm 279.8 ± 111.4 277.2 ± 110.3 269.5 ± 107.4 274.2 ± 110.4 277.4 ± 111.0 290.9 ± 115.8 286.9 ± 117.8 282.6 ± 112.2 279.5 ± 109.7
All eyes, μm 280.3 ± 106.1 274.9 ± 107.0 271.9 ± 103.5 274.3 ± 106.2 278.9 ± 104.7 290.8 ± 110.8 289.5 ± 110.9 282.3 ± 104.8 279.9 ± 103.9
Table 3.
 
Ocular Biometric Parameters and Fluctuations of Subfoveal Choroidal Thickness for Each Subject
Table 3.
 
Ocular Biometric Parameters and Fluctuations of Subfoveal Choroidal Thickness for Each Subject
Subject Age (y) Sex Eye RE (D) AL (mm) CCT (mm) Corneal Refraction (D) Total Mean S FCT (μm) (Mean ± SD) Min SFCT (μm/Time) Max SFCT (μm/Time) (Max − Min) SFCT (μm)
 1 37 M R −5.375 26.35 0.539 43 410.3 ± 17.6 384/6 PM 441/6 AM 57
L −4.875 26.19 0.542 42.75 398.8 ± 23.0 366/9 PM 431/3 AM 65
 2 31 M R −4.375 24.83 0.542 44.75 227.0 ± 5.96 218/Midnight 235/6 AM 17
L −3.25 24.07 0.54 44.75 304.8 ± 6.2 296/6 PM 315/3 AM 19
 3 28 M R −0.625 24.39 0.518 40.75 308.7 ± 11.3 284/9 PM 320/3 PM 36
L −0.125 24.27 0.521 40.75 324.2 ± 14.8 292/9 PM 337/9 AM 45
 4 44 M R −3.625 26.25 0.547 41.25 287.0 ± 7.9 276/9 PM 296/3 AM 20
L −4.625 26.78 0.543 41 168.8 ± 11.1 150/6 PM 182/6 AM 32
 5 39 M R −7.375 25.99 0.447 43.75 284.0 ± 13.6 259/3 PM 305/6 AM 46
L −7.375 25.99 0.447 43.5 289.2 ± 7.7 281/6 AM 300/6 PM 19
 6 28 F R −3.5 25.02 0.483 43.25 316.6 ± 9.2 299/Midnight 329/3 AM 30
L −5 25.65 0.478 43.25 241.5 ± 8.2 229/6 PM 252/3 AM 23
 7 29 F R −6.5 26.3 0.476 43.25 199.1 ± 16.5 169/6 PM 217/6 AM 48
L −6.25 26.2 0.483 43.25 196.8 ± 17.8 173/6 PM 225/3 AM 52
 8 38 M R −3.875 25.72 0.548 43.25 238.2 ± 17.2 199/3 PM 258/6 AM 58
L −4.25 26.05 0.55 43.25 221.5 ± 9.8 199/3 AM 231/9 PM 32
 9 50 M R −7.875 27.35 0.548 43.25 169.8 ± 8.6 159/3 PM 185/3 AM 26
L −7.25 26.72 0.536 43.25 179.7 ± 15.7 162/9 PM 209/3 AM 37
10 51 M R −2.75 26.42 0.493 40.5 164.0 ± 4.41 156/9 PM 167/9 AM 11
L −2.125 25.94 0.5 40.25 197.9 ± 5.2 188/9 PM 296/6 PM 8
11 27 M R −6.875 25.32 0.52 46.25 359.0 ± 7.71 347/6 PM 371/3 AM 24
L −5.5 25.16 0.53 46 354.2 ± 13.7 331/6 PM 379/6 AM 48
12 24 F R −4.125 25.37 0.552 43 258.7 ± 10.6 246/6 PM 275/6 AM 29
L −3.75 25.18 0.543 43.25 314.8 ± 10.4 304/6 PM 331/6 AM 27
13 27 F R −0.625 23.9 0.507 42.25 434.1 ± 17.7 412/Noon 449/6 AM 37
L −0.625 24.05 0.516 41.75 462.4 ± 19.5 436/6 PM 492/3 AM 56
14 36 F R −6 25.02 0.558 45 149.2 ± 11.7 136/9 PM 164/Midnight 28
L −5.75 24.58 0.555 45.25 115.1 ± 3.6 110/6 PM 119/3 AM 9
15 22 M R −5.75 25.28 0.521 44 285.1 ± 11.2 274/3 PM 308/3 AM 34
L −7.875 25.84 0.513 44.5 286.2 ± 7.84 272/6 PM 296/6 AM 24
16 47 F R 1.375 22.94 0.47 42.75 544.6 ± 14.9 523/9 AM 562/6 AM 39
L 0.75 23.18 0.475 42.75 557.8 ± 13.0 547/6 PM 584/6 AM 37
17 38 F R −3.625 25.38 0.475 42.5 326.0 ± 15.5 306/9 PM 351/3 AM 45
L −4.25 25.59 0.488 42.5 334.4 ± 14.4 319/Midnight 357/3 AM 38
18 37 F R −8.25 26.71 0.516 44.5 177.8 ± 8.0 167/9 AM 190/6 AM 23
L −6 26.03 0.503 44 180.4 ± 6.5 168/Noon 189/Midnight 21
19 29 F R −6.25 24.96 0.502 44.75 196.8 ± 7.1 188/Noon 206/6 AM 18
L −5.625 24.84 0.495 44.5 187.2 ± 5.8 183/6 AM 198/3 AM 15
Table 4.
 
Amplitude of Fluctuations in Subfoveal Choroidal Thicknesses
Table 4.
 
Amplitude of Fluctuations in Subfoveal Choroidal Thicknesses
SFCT Max SFCT − Min SFCT (μm), Mean ± SD Range (μm), Mean ± SD P *
Right eye 33.0 ± 13.4 26.5 ± 10.1 to 39.5 ± 19.8 <0.0001
Left eye 33.0 ± 15.5 25.4 ± 11.7 to 40.5 ± 23.0 <0.0001
All eyes 33.0 ± 14.3 28.3 ± 11.7 to 37.7 ± 18.5 <0.0001
Table 5.
 
Relationship between Subfoveal Choroidal Thickness and Other Systemic Factors
Table 5.
 
Relationship between Subfoveal Choroidal Thickness and Other Systemic Factors
Factor Right Eye Left Eye All Eyes
Coefficient R2 P Value Coefficient R2 P Value Coefficient R2 P Value
SBP −0.27 0.59 0.02* −0.27 0.53 0.04* −0.28 0.59 0.02*
DBP 0.07 0.06 0.54 0.01 0.002 0.90 0.04 0.02 0.70
MAP −0.04 0.03 0.64 −0.08 0.11 0.40 −0.06 0.07 0.51
HR −0.22 0.56 0.03* −0.17 0.29 0.16 −0.21 0.44 0.06
IOP −0.02 0.02 0.70 <0.01 <0.01 0.99 −0.01 <0.01 0.85
MOPP −0.02 0.02 0.72 −0.05 0.11 0.40 −0.03 0.04 0.61
Table 6.
 
Stepwise Regression Analysis for Influential Factors on Choroidal Thickness of All Eyes
Table 6.
 
Stepwise Regression Analysis for Influential Factors on Choroidal Thickness of All Eyes
Factor P
SBP 0.025*
DBP 0.48
MAP 0.48
HR 0.35
IOP 0.49
MOPP 0.88
Table 7.
 
Circadian Change of Systolic Blood Pressure (mm Hg) for Each Subject
Table 7.
 
Circadian Change of Systolic Blood Pressure (mm Hg) for Each Subject
Subject 3 PM 6 PM 9 PM Midnight 3 AM 6 AM 9 AM Noon
 1 127 130* 118 127 127 113† 116 126
 2 109 128* 118 108 120 128* 110 102†
 3 121* 116 114 113 112 104† 104† 110
 4 126 135* 115† 126 119 121 132 130
 5 117 122 125* 115 110† 122 116 122
 6 112* 106 109 100† 100† 107 102 107
 7 120* 113 117 113 110 104† 110 107
 8 109† 123 128* 112 109† 118 116 115
 9 136* 130 122 128 114† 123 116 134
10 181* 165 173 167 154 145† 173 180
11 113 112 115* 109 114 115* 96† 110
12 109 107† 120 115 128* 116 115 117
13 106* 96 104 92† 100 103 106* 101
14 114* 112 95† 110 109 100 99 110
15 126 115 119 103† 126 115 116 134*
16 119† 123 136 137* 130 120 123 135
17 107* 97 95 92† 94 95 94 100
18 115 118 113 120* 102 112 99† 107
19 104 121* 102 104 100† 105 100† 102
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