Does sunlight (bright lights) explain the protective effects of outdoor activity against myopia?

Authors


  • *All authors contributed equally to this paper.

Abstract

In the following point-counterpoint article, internationally-acclaimed myopia researchers were challenged to defend the two opposing sides of the topic defined by the title; their contributions, which appear in the order, Point followed by Counterpoint, were peer-reviewed by both the editorial team and an external reviewer. Independently of the invited authors, the named member of the editorial team provided an Introduction and Summary, both of which were reviewed by the other members of the editorial team. By their nature, views expressed in each section of the Point-Counterpoint article are those of the author concerned and may not reflect the views of all of the authors.

The notion that the diurnal cycles of light and dark influence ocular growth and refraction has been around for decades, going back to the work of Lauber and colleagues who showed that altered light cycles caused abnormal eye growth and refractive errors. In 1999, the controversy over the report that ambient night-time light led to the development of myopia in children[1-3] revived interest in this area. Subsequent work with potential implications for treatment therapies has shown that children who spend more time outdoors are at a lower risk of developing myopia than children who spend more time indoors.[4] A crucial question that awaits testing is whether the seemingly protective effects of time spent outdoors are mediated by light intensity and/or exposure time per se, or by some other aspect of the outdoor environment, such as the greater object distances outside compared to the restricted viewing distances inside. Here, Cheryl Ngo, Seang-Mei Saw and Ramamurthy Dharani present the evidence that exposure to bright light is the crucial factor, while Ian Flitcroft presents the opposing evidence that other aspects of being outdoors are critical.

Point

Myopia has reached epidemic levels in Asia, with prevalence rates of 28% in seven year olds in Singapore[5] and similarly high rates in other urban Asian cities. Current available data suggest the cause of myopia is multi-factorial, with interplay between genetic and environmental factors including time spent outdoors. Most intriguing is the protective role of increased outdoor time against myopia. A systemic meta-analysis of the association between time spent outdoors and myopia in children indicated a 2% reduced odds of myopia occurred per additional hour per week of time spent outdoors, after adjustment for covariates (OR, 0.98; 95% CI, 0.97–0.99; P < 0.001; I(2), 44.3%).[6] In a study amongst 6-year-old Chinese children, the prevalence rates were 29.1% in those living in Singapore, compared to 3.3% in children living in Sydney, Australia (p < 0.0001).[4] The main difference found was time spent outdoors, estimated to be 13.8 h week−1 in Sydney compared to 3.0 h week−1 in Singapore (p < 0.0001). The Sydney Myopia Study[4] and SCORM study[5] found that higher levels of outdoor activity were associated with lower prevalence rates of myopia. In a study amongst 681 1st and 4th grade Chinese children in Beijing, China, time spent outdoors had a protective association with myopia prevalence (OR: 0.32; 95% CI, 0.21–0.48, p < 0.001).[7] In the school-based Guangzhou Outdoor Activity Longitudinal (GOAL) Study on 1789 children aged 6.6 years (±0.34), preliminary results indicate that compared to children without intervention, those who had 1 h of scheduled time outdoors added to the school day had statistically significant reductions in refraction (0.86 ± 0.77 D vs 0.75 ± 0.69 D, p < 0.01) and axial elongation (0.61 ± 0.35 mm vs 0.59 ± 0.33 mm, p < 0.05) after 2 years.[8]

The protective effects of outdoor exposure appear more related to time outdoors than physical activity. Rose et al.[4] found that children who spent time outdoors had less myopia but playing indoor sports didn't help. In the ALSPAC Cohort study among 7–15 year old children, time spent outdoors predicted myopia onset independent of physical activity.[9] Children who spent lower time outdoors were 40% more likely to develop myopia, whilst children with low levels of physical activity were only 10% more likely to develop myopia.[9]

The most consistent mechanism shown by animal experiments, that underlie the association of time outdoors with myopia, is the light levels associated with outdoors. Animal studies have explored the effect of high ambient lighting on form deprivation[10-13] as well as lens induced myopia.[12, 13] In form deprivation myopia studies, chick eyes exposed to laboratory light of 15 000 lux for 5 h day−1 or sunlight of 30 000 lux for 15 min day−1 had significantly shorter eyes (8.81 ± 0.05 mm; P < 0.01) and less myopic refractions (−1.1 ± 0.45 D; p < 0.01), compared to chick eyes reared under normal laboratory illumination of 500 lux.[10] Ambient light levels as high as 18 000 to 28 000 lux also retarded form-deprivation myopia in infant monkeys and there was an 87% reduction in the average degree of myopic anisometropia in the high-light–reared monkeys.[11] Although high ambient lighting can retard the development of form deprivation myopia[10, 11] it only slows down the progression of lens induced myopia, and does not change the end point refraction.[13] After 11 days, tree shrews exposed to elevated light levels (around 16,000 lux for almost 8 hours) reduced form deprivation myopia by 44% (−3.6 ± 0.1 D vs −6.4 ± 0.7 D) and lens induced myopia by 39% (−2.9 ± 0.4 D vs −4.8 ± 0.3 D).[12] It has been proposed that an increased light intensity may trigger the release of dopamine, a light sensitive neuro-transmitter and ocular growth inhibitor.[13, 14] Injection of the dopamine antagonist, spiperone, abolished the protective effect of high light intensity in chick eyes with form deprivation myopia.[13]

In the FIT (Family Incentive Trial) study designed to increase outdoor time, we measured time and light levels indoors and outdoors in 117 Singapore children aged 6 to 12 years over a 1 week period.[15] Activities during the day were recorded with a diary, and corresponding light levels measured using a HOBO light meter worn on the wrist. The light levels in Lux measured outdoors were much higher than indoors. A recent study examined the association between myopia and time spent outdoors by measuring the UV absorption at conjunctiva using ultraviolet autofluorescence (UVAF), a biomarker of outdoor light exposure, in 636 young adults aged >15 years.[6] Total UV absorption was independently associated with myopia and prevalence of myopia decreased with an increasing quartile of total UVAF (p(trend) = 0.002) and with increasing time outdoors (p(trend) = 0.03). Such indirect measures of cumulative outdoor time could be useful in adult studies.

Possible differences in retinal luminance associated with different cone type densities in animal retinas may explain the protective effect of outdoor activity against myopia. Excessive blue-green wavelength in outdoor scenes may be protective against myopia.[16] In the average sunlit outdoor scene, there is a preponderance of blue light with some green light and a markedly decreased amount of red light.[16] Young chick eyes that were reared under excessive red light developed myopia when compared to chick eyes reared under excessive blue or white light.[17] Additions of blue light of >2 hours per day to 10 hours of red light induced hyperopia. A study on red-green colour vision deficiency in a group of school students found that the prevalence of myopia was significantly lower than a control group and it may be linked to the reduced functionality of the long/medium chromatic mechanism.[18] Further studies evaluating different wavelengths outdoors and indoors as well as clinical trials testing ‘blue light’ spectacles or headlamps could be implemented.

In summary, high ambient light levels have been found to influence the rate of form-deprivation myopia in animal models.[10, 11] Lens-induced myopia studies show slowed progression but no change in end point refractive error. These studies imply that the correlational protective effects of outdoor activities against myopia in children may be related to exposure to the higher light levels normally encountered in outdoor environments, and may be a fundamental variable controlling the vision-dependent regulation of ocular growth.

Counterpoint

Although several studies have previously noted a link between outdoor activities and myopia, this question has become a hot topic principally on the basis of a paper published in Ophthalmology in 2008.[4] This rapidly evolved into a renewed interest in light as the protective factor, though it is worth noting that in this 2008 paper no data relating to light was collected and the link is based entirely on the following speculative comment in the discussion – ‘We suggest that light intensity may be an important factor’.

Is light an important factor in refractive development? At one level of course, it is. We know the eye has very complicated growth control mechanisms, which being visually guided are inevitably dependent upon light. Has recent research into light and myopia opened up an exciting new avenue of investigation? Indeed it has but the position that bright light explains the (apparently) protective effects of being outdoors requires us to abandon decades of research into the control mechanisms of ocular growth. Over the last twenty years a vast body of research has demonstrated that this ocular growth process is visually guided and that local retinal defocus influences growth of the overlying sclera. Much of the initial work was done in the chick but it has now been demonstrated that the mammalian eye also responds to retinal defocus in a regional manner.[19, 20] There is now increasing evidence that the human eye is also sensitive to defocus, responding in the manner expected from animals studies.[21] The regulatory process of visually guided eye growth can be considered in engineering terms to be a closed feedback loop that serves to minimize retinal defocus and hence achieve and maintain emmetropia. In such terms light is an open loop stimulus. The total amount of light reaching the retina is unrelated and unaffected by the refractive state of the eye. If light does indeed help to prevent myopia and hence maintain emmetropia it must do so by influencing the operation of growth mechanisms that are closed loop. A study on Melanesian school children showed the majority (96.8%) to have a spherical equivalent refraction between −0.25 and +1.00 D.[22] Such high levels of emmetropia require axial length to be regulated within ±250 μm so as to match the very variable optical properties of the anterior segment. This is a true feat of biological homeostasis that could only be achieved with a closed loop control system.

Does light impact upon the control mechanisms of eye growth? Yes it does. Animal studies have indicated that lower light intensities slow the relative speed of responses to negative lenses (hyperopic blur) as compared to positive lenses (myopic blur) without changing the set-point of emmetropisation, an effect blocked by a dopamine antagonist.[13] Emmetropisation was also found to be slower in low light in another study, though all groups showed surprisingly slow emmetropisation, taking 30-50 days even in the bright light group.[14] In the dimmest light group (50 lux), chicks became myopic by 90 days,[14] while constant darkness results in significant increases in eye growth within mere days.[23] In monkeys deprivation myopia is protected by both low light[24] and very bright light (25 000 lux).[11] Such findings indicate that light can certainly modulate ocular growth mechanisms, but that doesn't mean we can forget the central role such mechanisms play in eye growth.

Let's look at the differences between indoors and outdoors. Yes, indeed there is more light outdoors. But in terms of the major stimulus known to influence eye growth, i.e. retinal defocus, the major difference between indoors and outdoors is the structure of the visual environment. The structure of the environment indoors has relatively little impact on foveal defocus due to the operation of the accommodation system (another closed feedback loop), but peripherally it induces a wide range of both myopic and hyperopic errors depending on the task being performed.[25] These optical differences are influenced by light level since bright light reduces pupil size and hence alters depth of focus, but in this regard light is once again impacting upon the function of the underlying control system. Outdoors the visual environment is optically far more uniform and in growth terms provides a stop signal, as there is no significant level of defocus across the visual field. In contrast all indoor activities – reading, computer use or looking at a more distant point indoors – create large amounts of peripheral defocus so there is no activity which provides an in-focus stop signal across the retina. Furthermore, irrespective of the specific task or fixation point, all indoor activities create far more hyperopic defocus than is observed outdoors. As there are potential optical benefits of being outdoors and optical risks of being indoors, not being indoors may be just as important as being outdoors. If bright light is affecting the visually guided control mechanisms of eye growth in humans, as has been demonstrated in animals, then it is essential to consider the optical differences between the indoor and outdoor environments as retinal defocus has been found to be a critical component of visually guided eye growth.

A further major caveat relating to the question posed above is the inherent assumption that the observed association between time outdoors is indeed protective for human myopia. To be valid this requires evidence of causation, which is currently lacking. The epidemiology of myopia is full of statistical associations that have proved difficult to decipher including education, occupation, socio-economic status and intelligence. Based on just such associations making sure our children have a low socio-economic status and a poor education would also be an effective strategy to limit myopia.

I want to end this analysis with a quote from H. L. Mencken, ‘For every complex problem, there is a solution that is simple, neat, and wrong.’ Over the years there have been many simple and neat theories to explain myopia that have been proved wrong. I think few would argue with the statement that myopia is a complex phenomenon. Before jumping on the ‘light bandwagon’ we should bear this in mind.

Summary

Debora Nickla

Department of Biomedical Sciences and Disease, New England College of Optometry,Boston, USA

E–mail:NicklaD@neco.edu

Points of Agreement

  • An association between time outdoors and myopia has been a consistent finding in epidemiological studies of children.
  • Light levels have been shown to influence refractive development in several animal models.
  • Sunlight differs from indoor lighting in its spectral composition as well as its brightness, which may influence the availability of defocus cues used by the emmetropisation system.

Issues to be Resolved

  • Is the observed association between time outdoors and myopia development causal, or a result of confounding factors? On-going randomised controlled trials should address this question, and indeed quantify the magnitude of any protective effect.
  • Since the emmetropisation system appears able to distinguish the ‘sign of defocus’ of the retinal image, how does the absolute light level interact with this defocus-detection mechanism (and is this conserved across species)?
  • Outdoors versus indoors, the level and uniformity of defocus across the whole retina is dramatically different. Is this difference, rather than brightness, the reason for any protective effect of time outdoors?

Biographies

  • Image of creator

    Cheryl Ngo

  • Image of creator

    Seang-Mei Saw

  • Image of creator

    Ramamurthy Dharani

  • Image of creator

    Ian Flitcroft

Ancillary