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Abstract
Aim To evaluate the short-term effects of different sunlight exposure on fundus blood flow perfusion (BFP) after near work.
Methods In this parallel randomised controlled trial, 81 students aged 7–15 with spherical equivalent refraction between −2.00 and +3.00 diopters were randomly assigned to either a low-illuminance (4k lux) group (N=40) or high-illuminance (10k lux) (N=41). Following 1 hour indoor reading, participants had sunlight exposure matching their group’s intensity for 15 minutes. BFPs in the superficial retina, deep retina and choroid were measured at four time points: pre-reading, post-reading, 5th-minute and 15th-minute sunlight exposure.
Results Within the initial 5 minutes of sunlight exposure, the 10k lux group showed a tendency for decreased BFP, particularly in the choroid (superficial retina: −0.2, 95% CI −0.9 to 0.5; deep retina: −0.1, 95% CI −0.6 to 0.4; choroid: −0.4, 95% CI −0.8 to 0.0), while the 4k lux group exhibited an increase (superficial retina: 0.7, 95% CI 0.1 to 1.3; deep retina: 0.3, 95% CI −0.2 to 0.8; choroid: 0.1, 95% CI −0.2 to 0.5). From 5 to 15 minutes, BFP decreased in both groups. At the 5th-minute mark, the 10k lux group exhibited a greater decrease in choroid (10k −0.4 vs 4k 0.1, p=0.051). No significant difference was observed after 15 minutes of exposure.
Conclusion Higher illuminance sunlight exposure can restore fundus BFP more rapidly than lower; however, duration remains pivotal. To prevent myopia, continuous sunlight exposure for over 15 minutes is recommended to aid in reinstating the fundus BFP increased by near work.
Trial registration number NCT05594732.
- Retina
- Choroid
- Optics and Refraction
- Physiology
- Clinical Trial
Data availability statement
Data are available upon reasonable request. No data are available. No additional unpublished data from the study are available.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
Prolonged sunlight exposure plays a role in myopia prevention in the long term, while the short-term effects of sunlight exposure on fundus blood flow remains unknown.
WHAT THIS STUDY ADDS
Sunlight exposure can decrease fundus blood flow perfusion increased by near work in an intensity- and time-dependent manner, with choroidal perfusion being the most sensitive.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
To prevent myopia, continuous exposure to sunlight for 15 minutes or more is recommended to aid in reinstating the fundus blood flow increased by near work.
Introduction
Myopia has emerged as a widespread global concern. According to the WHO report of 2023, approximately 2.2 billion people worldwide were affected by vision impairment, with over 1 billion cases being potentially preventable, and the leading cause being refractive errors.1 Notably, the prevalence of myopia among Chinese school-aged children in 2020 was 53%.2 This increasing trend highlights the pressing need for immediate attention and proactive preventive strategies.
Previous research has conclusively demonstrated that increased intensity and duration of sunlight exposure can effectively reduce the risk of developing myopia.3 4 Various randomised controlled trials conducted in different regions of the world have provided compelling evidence of the protective role of prolonged sunlight exposure.5–10 A comprehensive systematic review and meta-analysis conducted in 2019, involving 15 081 children aged 4–14 from 13 studies, revealed a direct correlation between sunlight exposure duration and a decrease in myopia incidence, highlighting a clear dose–response relationship.11 Moreover, alongside sunlight exposure duration, studies have indicated a negative association between lower ambient light levels and the prevalence of myopia, as well as a notable link between reduced sunlight exposure intensity and the onset of myopia.12 13 Although the long-term benefits of sunlight exposure in preventing myopia have been established, the immediate effects of sunlight exposure on ocular parameters for myopia prevention remain incompletely understood.
Altered fundus blood flow is considered to play a role in the pathogenesis of myopia and can serve as a predictive indicator for myopia development.14 15 This critical physiological parameter is intricately linked to ocular health and visual function, playing a pivotal role in maintaining fundus homeostasis and facilitating the delivery of essential nutrients and oxygen.16 Clinical studies have demonstrated that individuals with myopia often exhibit diminished choroidal and retinal blood flow perfusion (BFP), contributing to scleral hypoxia and subsequent myopia progression.17 18 Animal studies also observed a change in the myopic eye compared with the fellow eye, and actively control the fundus vessels could affect the course of myopia development, which add to the evidence of the role of fundus blood flow played in myopia pathogenesis.19 20 Although the focuses of these studies also were the long-term change of myopia, they at least pointed to the fact that fundus blood flow was a promising direction in exploring myopia pathogenesis. The gap that studies on the immediate change of fundus blood flow after myopic stimulus and sunlight exposure was lacking should be filled. Therefore, it is postulated that fundus BFP could serve as a short-term predictive indicator for myopia. Investigating the correlation between sunlight exposure and fundus BFP can aid in identifying effective sunlight exposure patterns for myopia prevention.
This study aims to explore the relationship between sunlight exposure and fundus BFP, particularly focusing on the changing trend of BFP under different sunlight exposure intensities. The findings can significantly contribute to identifying the effective sunlight exposure patterns on myopia prevention and optimising outdoor interventions strategies.
Methods
Study design
This was a parallel randomised controlled trial conducted in Shanghai Eye Disease Prevention and Treatment Center from August to September 2022. Participants were asked to read books at a distance of 33 cm for 1 hour in an indoor environment with 2000 lux after basic eye examinations and then had sunlight exposure for 15 minutes by randomly grouping into two groups, the low-illuminance (4k lux) group or high-illuminance (10k lux) group. The flowchart presented the study design for the current study (figure 1). The trial protocol is shown in online supplemental material.
Supplemental material
Flow chart of the study design. BFP, blood flow perfusion.
Participants
Participants were recruited through both online and offline postings. Before official enrolment, they underwent non-cycloplegic autorefraction tests. If their results, along with responses to questionnaires, met the inclusion criteria, they were randomly assigned to either group using a random number table generated by Excel and allocated according to the odevity. Inclusion criteria consisted of the following: (1) aged from 7 to 15, (2) had a spherical equivalent refraction (SER) between −2.0 D and +3.0 D with astigmatism less than 0.75 D in the dominant eye and (3) willing to participate in the study. Exclusion criteria encompassed conditions such as amblyopia, strabismus, colour vision deficiency, congenital cataract, glaucoma or other ocular disorders, as well as any circumstances deemed unsuitable for participation by the investigator.
Measurements
Basic demographic information was gathered through a questionnaire. The dominant eye was identified. Best-corrected visual acuity was evaluated using the ETDRS Log MAR E scale (Precision Vision, Villa Park, Illinois, USA) at a distance of 4 m. Non-cycloplegic refraction was conducted using an autorefractor (Topcon KR8900, Japan) in three consecutive measurements, and the average was used for analysis. Measurements of axial length (AL), anterior chamber depth, central corneal thickness and lens thickness were obtained with the IOL Master 700 (Carl Zeiss Meditec, Germany). Non-contact optical tension was measured using a non-contact tonometer (NT-510, Nidek, Japan). The fundus BFP was obtained with AngioVue optical coherence tomography angiography (OCTA) Imaging System (Optovue, Fremont, USA) to quantitatively measure parameters of panretinal blood flow density with AngioAnalytics, select blood vessel complexes in the superficial and deep retina, as well as the choroid, and calculate the proportion of the corresponding area occupied by the blood flow signal. The lighting conditions were assessed using an illuminance metre (SIS-20, EVERFINE, China). Symptoms experienced during and after near work were collected via visual comfort questionnaires. All assessments were conducted by trained and experienced investigators blinded from the grouping. Data from eye examinations were entered into an online information system with built-in logic verification features. Questionnaire results and environmental monitoring data were also independently input by two investigators into the information system for verification.
Outcomes
BFPs of the superficial retina, deep retina and choroid of two eyes was examined at four different time points for each person: pre-reading, post-reading, 5th-minute sunlight exposure and 15th-minute sunlight exposure. The changes of BFP of macular zone in superficial retina, deep retina, and choroid in the dominant eye were calculated to describe the change trend of BFP and compare the difference between the low-illuminance (4k lux) group or high-illuminance (10k lux) group. A repeatability test was conducted among additional nine participants to confirm the stability and accuracy of BFP examination with OCTA (see online supplemental table 1 and figure 1).
Supplemental material
Supplemental material
Sample size
There were few studies reported the values of fundus BFP under different sunlight exposures. Based on a similar study and pilot test,21 it was determined that the estimated sample size needed for the study was 46 participants at least, with 23 individuals allocated to each group. This calculation was based on a significance level of 0.05, a desired statistical power of 90%, a minimum expected difference in superficial retina BFP changes of 1.5% (2.5% vs 1.0%) following 15 minutes of sunlight exposure, with an SD of 1.5% within the group, and an equal allocation ratio of 1:1. To ensure that the study maintained the desired statistical power, a total of 81 children were ultimately recruited and investigated.
Statistical analysis
The analysis included the fundus BFP of the dominant eye. Descriptive statistics, such as mean and SD, were used to describe continuous variables, which included age, height, weight, AL, SER, non-contact tonometry, and BFP in various layers. Categorical variables were summarised using frequencies and percentages. To compare the differences between the two groups, a t-test for two independent samples was applied. A paired t-test was used to assess differences within the same group at different time points. Linear mixed models were applied to compare the BFP between different time points within each group of sunlight exposure. For all comparisons, the 95% CIs and p values were calculated. A repeatability test with Bland-Altman analysis was conducted to evaluate the stability and accuracy of OCTA examination. Data cleaning and analysis were conducted using the commercial software SAS (V.9.4, SAS Institute) and R (V.4.2.3).
Results
Baseline characteristics
Figure 1 showed an overview of the participants’ enrolment, allocation, examination and interventions. In total, 81 students were included, 41 in the 10k lux group and 40 in the 4k lux group. Table 1 presented the basic characteristic of the students included. The mean age was 10.2±2.1 years in each group. The height and weight were similar in both groups (144.9±15.4 cm vs 143.6±13.1 cm, p=0.681; 40.7±14.6 kg vs 38.1±12.0 kg, p=0.390). The mean AL was 24.1±1.1 mm in the 10k lux group and 23.7±0.9 mm in the 4k lux group, and SER was −0.80±1.40 D and −0.70±1.50 D, respectively, suggesting comparable refractive status between two groups (p=0.060 and 0.782). The fundus BFP at superficial retina, deep retina and choroidal layers was comparable at baseline between the two groups (p=0.468, 0.068 and 0.354).
Characteristics of participants in 10k lux and 4k lux group
Changes of fundus BFP at different time points
The fundus BFP and its change at different time points in the study were presented in table 2, figures 2 and 3. In general, the BFP increased following near work and decreased after exposure to sunlight. Analysing the changing trends across the three different layers, within the initial 5 minutes of exposure to sunlight, a decrease in fundus BFP was evident in the 10k lux group across all three layers (superficial retina: −0.2, 95% CI −0.9 to 0.5; deep retina: −0.1, 95% CI −0.6 to 0.4; choroid: −0.4, 95% CI −0.8 to 0.0). In contrast, the 4k lux group displayed a continued increase in fundus BFP (superficial retina: 0.7, 95% CI 0.1 to 1.3; deep retina: 0.3, 95% CI −0.2 to 0.8; choroid: 0.1, 95% CI −0.2 to 0.5) during the same period. Subsequently, within the second interval, spanning from 5 to 15 minutes of sunlight exposure, BFP decreased in both the 10k lux and 4k lux groups.
Blood flow perfusion of different layers in 10k lux and 4k lux group at different time points
Blood flow perfusion of different fundus layers in 10k lux and 4k lux group at different time points. The red point indicated the group of 10k lux, and the green point indicated the group of 4k lux. The bar indicated the two standard deviationsSD.
Change of blood flow perfusion of different fundus layers in 10k lux and 4k lux group compared tocompared with the value after reading. The value of blood flow perfusion at post-reading was set as the reference to show the change trend. The red point indicated the group of 10k lux, and the green point indicated the group of 4k lux. The bar indicated 95% confidence intervalCI of mean. P values were for the comparisons of differences of change between 10k lux and 4k lux group.
Comparison of fundus BFP changes between the 10k lux and 4k lux groups
As depicted in table 3 and, there were no significant differences in retinal blood flow changes between the two groups before and after reading. Five minutes after exposure to sunlight, the 10k lux group exhibited a greater decrease in choroidal BFP change compared with the 4k lux group with marginal significance (10k lux: −0.4 vs 4k lux: 0.1, p=0.051). Nevertheless, at the 15th minute after exposure to sunlight, there was no significant difference in choroidal BFP change between the 10k lux and 4k lux groups. Either it was at the 5th minute or 15th minute of sunlight exposure, the changes of superficial retinal BFP between the 10k lux and 4k lux groups was different (10k lux vs 4k lux: 0.3 vs −0.4, p=0.058; 10k lux vs 4k lux: −0.2 vs 0.2, p=0.064), with 4k lux group’s BFP not recovering to the pre-reading state. However, no significant differences were detected in deep retinal BFP changes between the two groups at the 5th minute and 15th minute of sunlight exposure.
Changes of blood flow perfusion of different layers at different time points
Discussion
Our study found that exposure to sunlight could mitigate the elevation of BFP caused by near work. Sunlight of higher intensity could efficiently contribute to the recovery of BFP after near work, while the prolonged duration of sunlight exposure was equally essential for both high and low light intensities in reinstating BFP. These findings provided valuable insights into the potential of sunlight exposure patterns in strategies for myopia prevention.
Exposure to sunlight, especially at higher intensities, efficiently countered the elevation of fundus BFP induced by near work such as continuous reading a book for 1 hour. The effect of continuous near work, which might be a myopia stimulus, on fundus blood flow seemed opposite to the previous knowledge that myopic eyes have decreased fundus blood flow. This brought to the differences in the long-term change and immediate change. The retina, being the most oxygen-consuming and sensitive tissue in the body, relies on retinal and choroidal capillary perfusion for oxygen supply.22 Previous studies indicate that during visual signal processing, the retina demands increased energy, leading to elevated oxygen consumption and subsequent augmented blood flow to meet these heightened requirements.23 Retinal blood flow increases to compensate for hypoxia, in order that oxygen delivery is maintained relatively constant, as a physiological process.24 This aligns with our observations in this study, as the BFP in both the retinal and choroidal layers increased after 1 hour of intense near work. Conversely, in the outdoor environment with less visual processing, in conjunction with the effects of sunlight, the demand for oxygen decreased, resulting in reduced perfusion levels. Notably, 10k-lux sunlight could swiftly reverse the choroidal BFP within 5 minutes, which was not observed with 4k-lux sunlight. This disparity underscores the significant role of sunlight intensity in mitigating BFP. While weak sunlight may not restore BFP within the initial 5 minutes, we did observe its restorative impact over the entire 15 minutes’ duration, suggesting that exposure to low sunlight intensity could still gradually reinstate the retinal BFP, although at a slower pace. The initial 5 minutes’ rise in BFP at the 4k lux group may be attributed to the delayed impact of near work. One recent study found that after near work for 40 minutes, the choroidal capillary perfusion decreased, which was contrary to our findings.25 The variation can be attributed to the contrasting age groups of the participants; the former study involved young adults aged 19–28 years, whereas our study comprised students aged 8–15 years. Since the choroidal circulation is different between children and adults, and this contributed to opposite response to near work.26
A comparison across the three different layers revealed that the choroidal BFP recovered more rapidly, while the retinal BFP restoration was comparatively slower, indicating the heightened sensitivity of the choroid layer to oxygen demands and blood flow provision. This disparity in the changes in superficial and deep retinal blood flow density has been previously documented.27–29 The different changes of the two layers in various light environments were due to the different part of photoreceptors vessels in the two layers supplied to, and the dual blood supply from the retinal and choroid vasculature added to the complexity, but the final goal was to adjust the blood flow to the oxygen needs.30 31 Animal studies have demonstrated that oxygen levels are highest near the choroid and decrease towards the superficial retina.32 Thus, it is plausible that the varying oxygen requirements and uneven distribution of blood vessels contribute to the distinct recovery rates of BFP in the retina and choroid layers.33 Our findings suggest that changes in choroidal BFP can serve as a sensitive indicator of sunlight exposure.
Furthermore, the study indicated that besides sunlight intensity, the duration of sunlight exposure is pivotal in restoring BFP. We observed that the BFP in the retina and choroid gradually returned to their pre-reading status after continuous exposure to sunlight for 15 minutes, particularly notable in the choroid BFP for both the 10k-lux and 4k-lux groups. Various studies have established a correlation between myopia and the thickness of different areas in the choroid and retina, along with vessel densities,34 with several studies exploring the influence of the choroid on the onset and progression of myopia.17 Insufficient duration of continuous sunlight exposure may hinder the immediate recovery of fundus BFP, potentially leading to prolonged oxygen deficiency. Therefore, a continuous exposure to sunlight for at least 15 minutes, especially under low sunlight intensity environments, is recommended.
There are some limitations as the sunlight exposure only lasted for 15 minutes, and we only compared two sunlight intensities. Also, despite supervision, some participants might be distracted when doing the 1-hour near work, which might affect the post-reading fundus BFP at the beginning, decreasing the significance level of the changes after sunlight exposure. Finally, variations in the systolic blood pressure could have an impact on the retinal and choroid blood vessels, resulting in changes of the fundus BFP.35–37 However, this confounding factor was not included in the analysis, which may introduce a potential bias for the results.
In conclusion, our study emphasises that sunlight exposure can effectively counter the increase in fundus BFP due to near work. Sunlight with higher illuminance can restore fundus blood flow more rapidly than lower illuminance, but the duration of exposure remains a critical factor. To prevent myopia, continuous exposure to sunlight for 15 minutes or more is recommended to aid in reinstating the fundus blood flow increased by near work.
Data availability statement
Data are available upon reasonable request. No data are available. No additional unpublished data from the study are available.
Ethics statements
Patient consent for publication
Ethics approval
This study involves human participants and was approved by Clinical Trial Ethics Committee of Shanghai Eye Disease Prevention and Treatment Center (No. EC-20220823-06). Both participants and their guardians gave informed consent to participate in the study before taking part.
References
Footnotes
Funding This study was supported by Excellent Academic Leader of Shanghai Science and Technology Commission (22XD1422900).
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
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