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Spectral modulation of light wavelengths using optical filters: effect on melatonin secretion

2014; Elsevier BV; Volume: 102; Issue: 2 Linguagem: Inglês

10.1016/j.fertnstert.2014.06.006

1556-5653

Robert F. Casper, Shadab A. Rahman,

Spaceflight effects on biology

Shiftwork has been identified as a risk factor for various medical problems, such as cancer, heart disease, metabolic disturbances, depression, and anxiety disorders, and as reviewed this month, adverse reproductive function. Shiftwork misaligns physiological rhythms with respect to each other and to external environmental rhythms such as the 24-hour light/dark cycle. Light is the strongest time cue for entraining circadian rhythms in mammals, and aberrant light exposure patterns during shiftwork is one of the key factors that induce circadian misalignment. We have recently demonstrated, in both animal and clinical models, that filtering short wavelengths (below 480 nm) from nocturnal lighting can attenuate alterations in hormone secretion (melatonin and glucocorticoids) and in central and peripheral clock gene expression induced by nighttime light exposure. We also demonstrated that the use of optical filters led to an improvement in mood and in cognitive performance under controlled laboratory conditions and during field-based shiftwork studies. Moreover, there was an increase in sleep duration and quality on nights immediately following night shifts. We believe it is likely that optical filters incorporated into glasses or as coverings for light bulbs could be used as a method to improve or prevent many of the medical problems associated with circadian misalignment and rotating shiftwork. Shiftwork has been identified as a risk factor for various medical problems, such as cancer, heart disease, metabolic disturbances, depression, and anxiety disorders, and as reviewed this month, adverse reproductive function. Shiftwork misaligns physiological rhythms with respect to each other and to external environmental rhythms such as the 24-hour light/dark cycle. Light is the strongest time cue for entraining circadian rhythms in mammals, and aberrant light exposure patterns during shiftwork is one of the key factors that induce circadian misalignment. We have recently demonstrated, in both animal and clinical models, that filtering short wavelengths (below 480 nm) from nocturnal lighting can attenuate alterations in hormone secretion (melatonin and glucocorticoids) and in central and peripheral clock gene expression induced by nighttime light exposure. We also demonstrated that the use of optical filters led to an improvement in mood and in cognitive performance under controlled laboratory conditions and during field-based shiftwork studies. Moreover, there was an increase in sleep duration and quality on nights immediately following night shifts. We believe it is likely that optical filters incorporated into glasses or as coverings for light bulbs could be used as a method to improve or prevent many of the medical problems associated with circadian misalignment and rotating shiftwork. Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/casperr-spectral-modulation-light-optical-filters-melatonin/Shiftwork is an underpinning of the economy of all industrialized nations. Shiftworkers abound in the healthcare and manufacturing sectors and in almost all other industries. In fact, there are more than 13 million shiftworkers in North America alone. Unfortunately, shiftwork has been identified as a potential risk factor for various medical problems, such as cancer, heart disease, metabolic disturbances, and depression and anxiety disorders (1Hansen J. Risk of breast cancer after night—and shift work: current evidence and ongoing studies in Denmark.Cancer Causes Control. 2006; 17: 531-537Google Scholar, 2Martino T.A. Tata N. Belsham D.D. Chalmers J. Straume M. Lee P. et al.Disturbed diurnal rhythm alters gene expression and exacerbates cardiovascular disease with rescue by resynchronization.Hypertension. 2007; 49: 1104-1113Google Scholar, 3Gomez-Abellan P. Hernandez-Morante J.J. Lujan J.A. Madrid J.A. Garaulet M. Clock genes are implicated in the human metabolic syndrome.Int J Obes (Lond). 2008; 32: 121-128Google Scholar, 4Srinivasan V. Smits M. Spence W. Lowe A.D. Kayumov L. Pandi-Perumal S.R. et al.Melatonin in mood disorders.World J Biol Psychiatry. 2006; 7: 138-151Google Scholar). The previous two reviews by Reiter et al. (5Reiter R.J. Tan D.X. Galano A. Melatonin and the circadian system: contributions to successful female reproduction.Fertil Steril. 2014; 102: 321-328Abstract Full Text Full Text PDF Scopus (131) Google Scholar) and by Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar) have also described the adverse effects of altered lighting schedules on reproductive function including ovulatory and placental function, and the onset of labor, respectively. Most of the health disorders associated with shiftwork can be attributed to unavoidable chronic sleep deficiency and recurrent circadian rhythm disruption. Numerous physiological functions exhibit a circadian (∼24 hours) profile, and these can be broadly divided into molecular, endocrine, and behavior/activity rhythms. Disruption of circadian rhythms is common in shiftworkers, with exposure to nocturnal lighting being the most important disruptive factor.Shiftwork misaligns physiologic rhythms with respect to each other and to external environmental rhythms such as the 24-hour light/dark cycle. The most common approach to counteract the adverse health effects of light exposure during night shiftwork has been to alter the internal circadian phase of subjects such that the new rhythm matches the altered light/dark cycle during shiftwork. In other words, attempts have been made to invert circadian rhythms by exposure to bright light at night and exposure to darkness during the day. Several studies have shown that combined use of bright light at night and dark goggles that reduce light intensity and short-wavelength light transmission during the day may facilitate circadian adaptation to permanent night shiftwork (7Boivin D.B. Boudreau P. Tremblay G.M. Phototherapy and orange-tinted goggles for night-shift adaptation of police officers on patrol.Chronobiol Int. 2012; 29: 629-640Google Scholar, 8Sasseville A. Hebert M. Using blue-green light at night and blue-blockers during the day to improve adaptation to night work: a pilot study.Prog Neuropsychopharmacol Biol Psychiatry. 2010; 34: 1236-1242Google Scholar). However, an inversion of the circadian rhythm is seldom achieved outside of laboratory conditions, even across successive night shifts and after years of night work experience (9Costa G. Shift work and occupational medicine: an overview.Occup Med (Lond). 2003; 53: 83-88Google Scholar). One of the reasons this simple strategy fails in practice may be unavoidable exposure to bright light in the morning during the home commute after the night shift, or during weekends (10Boivin D.B. Czeisler C.A. Resetting of circadian melatonin and cortisol rhythms in humans by ordinary room light.Neuroreport. 1998; 9: 779-782Google Scholar).We, and others, have shown that selectively removing wavelengths shorter than ∼500 nm from nocturnal illumination prevents melatonin suppression induced by light exposure at night (8Sasseville A. Hebert M. Using blue-green light at night and blue-blockers during the day to improve adaptation to night work: a pilot study.Prog Neuropsychopharmacol Biol Psychiatry. 2010; 34: 1236-1242Google Scholar, 11Kayumov L. Casper R.F. Hawa R.J. Perelman B. Chung S.A. Sokalsky S. et al.Blocking low-wavelength light prevents nocturnal melatonin suppression with no adverse effect on performance during simulated shift work.J Clin Endocrinol Metab. 2005; 90: 2755-2761Google Scholar, 12Sasseville A. Paquet N. Sevigny J. Hebert M. Blue blocker glasses impede the capacity of bright light to suppress melatonin production.J Pineal Res. 2006; 41: 73-78Google Scholar). We have recently demonstrated, in an animal model, that filtering a narrow range of wavelengths (between 450 and 480 nm) from nocturnal lighting can attenuate alterations in hormone secretion (melatonin and corticosterone) and in central and peripheral clock gene (Per2 and Bmal-1) expression (13Rahman S.A. Kollara A. Brown T.J. Casper R.F. Selectively filtering short wavelengths attenuates the disruptive effects of nocturnal light on endocrine and molecular circadian phase markers in rats.Endocrinology. 2008; 149: 6125-6135Google Scholar). We extended these studies to humans in a simulated night shiftwork environment. Thirteen normal volunteers, who were screened to rule out any sleep dysfunction, were kept either in darkness, bright light (fluorescent ∼800 lux), or filtered bright light (fluorescent ∼800 lux while wearing glasses fitted with optical filters to block all wavelengths below 480 nm) for the entire duration of the study between 2000 and 8000 hours.In addition, in a fourth night study, light was filtered using identical glasses fitted with commercially available color-tinted lenses (placebo). Exposure to light at night suppressed the nocturnal rise in melatonin (Fig. 1), increased cortisol secretion, and shifted the expression of the clock genes Per2 and Bmal-1 (14Rahman S.A. Marcu S. Shapiro C.M. Brown T.J. Casper R.F. Spectral modulation attenuates molecular, endocrine and neurobehavioral disruption induced by nocturnal light exposure.Am J Physiol Endocrinol Metab. 2011; 300: E518-E527Google Scholar). Although the placebo filters were ineffective, filtering wavelengths below 480 nm from polychromatic white light was successful in preventing melatonin suppression (Fig. 1), cortisol elevation, and circadian disruption of clock gene expression by light at night (14Rahman S.A. Marcu S. Shapiro C.M. Brown T.J. Casper R.F. Spectral modulation attenuates molecular, endocrine and neurobehavioral disruption induced by nocturnal light exposure.Am J Physiol Endocrinol Metab. 2011; 300: E518-E527Google Scholar). Furthermore, there were no significant differences in alertness, sleepiness, fatigue, or vigilance after restoring normal melatonin secretion using filtered light exposure. One drawback of these lenses is a slight yellow hue that sharpens visual acuity by increasing contrast, but may make recognition of a few colors problematic.We followed this laboratory trial with a field study in nurses working a rapid rotation night/day shift schedule and confirmed the beneficial hormonal effects of filtering out short wavelengths from light at night (15Rahman S.A. Shapiro C.M. Wang F. Ainlay H. Kazmi S. Brown T.J. et al.Effects of filtering visual short wavelengths during noctural shiftwork on sleep and performance.Chronobiol Int. 2013; 30: 951-962Google Scholar). We also demonstrated improved sleep duration and quality by polysomnography (PSG) on nights immediately following night shifts. There was an improvement in mood and cognitive performance toward the end of the night shift with the use of the optical filters as well (15Rahman S.A. Shapiro C.M. Wang F. Ainlay H. Kazmi S. Brown T.J. et al.Effects of filtering visual short wavelengths during noctural shiftwork on sleep and performance.Chronobiol Int. 2013; 30: 951-962Google Scholar).With this new information that disruptions in circadian phase markers can be attenuated or prevented by eliminating short wavelengths from light at night, it may be possible to attenuate circadian misalignment, and the optical filters can be used as a method to improve or prevent many of the adverse medical changes associated with shiftwork. For female shiftworkers, allowing normal melatonin secretion at night might prevent the increased risk of breast cancer, metabolic problems such as insulin resistance, and depression and sleep disturbances. Specifically with regard to this month's View and Reviews focus on reproduction, another speculation is that reproductive function could be improved by using optical filters in women exposed to light at night. For example, the restoration of melatonin rhythms by filtering short-wavelength light could improve follicle development and ovulatory function as suggested by Reiter et al. (5Reiter R.J. Tan D.X. Galano A. Melatonin and the circadian system: contributions to successful female reproduction.Fertil Steril. 2014; 102: 321-328Abstract Full Text Full Text PDF Scopus (131) Google Scholar). If melatonin plays a role in placental function and fetal development, there could also be a beneficial effect on the pregnancy, although future studies are required to investigate these hypotheses.Similarly, the onset of labor is usually nocturnal, likely because of the synergistic effect of melatonin on oxytocin receptors as described by Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar). Their fascinating demonstration that exposure of women in labor to bright light for as little as 1 hour was capable of inhibiting contractions supports the possible synergistic effect of melatonin and oxytocin. To extrapolate these findings clinically, one could hypothesize that when women are admitted to the hospital in labor at night, exposure to overhead lighting could inhibit uterine contractions by suppressing melatonin levels, thus prolonging the time to the second stage of labor. In this situation, we speculate that the use of optical filters that block short-wavelength light could have beneficial effects by preventing the suppression of melatonin and allowing labor to progress normally with maintenance of the quality and strength of contractions and shortening of the latent and active phases of labor. On the other hand, Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar) suggest that some women enter premature labor because of the early induction of melatonin receptors in the myometrium. In these women, exposure to light at night, and suppression of melatonin secretion, could have a favorable effect in inhibiting contractions.Taken together, all of the described studies suggest that the invention of the electric light, while enhancing our lives in many ways, may also have deleterious effects on several aspects of human health, including reproductive function. Filtering or removing short wavelengths from light may potentially abrogate these deleterious effects. Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/casperr-spectral-modulation-light-optical-filters-melatonin/ Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/casperr-spectral-modulation-light-optical-filters-melatonin/ Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/casperr-spectral-modulation-light-optical-filters-melatonin/ Shiftwork is an underpinning of the economy of all industrialized nations. Shiftworkers abound in the healthcare and manufacturing sectors and in almost all other industries. In fact, there are more than 13 million shiftworkers in North America alone. Unfortunately, shiftwork has been identified as a potential risk factor for various medical problems, such as cancer, heart disease, metabolic disturbances, and depression and anxiety disorders (1Hansen J. Risk of breast cancer after night—and shift work: current evidence and ongoing studies in Denmark.Cancer Causes Control. 2006; 17: 531-537Google Scholar, 2Martino T.A. Tata N. Belsham D.D. Chalmers J. Straume M. Lee P. et al.Disturbed diurnal rhythm alters gene expression and exacerbates cardiovascular disease with rescue by resynchronization.Hypertension. 2007; 49: 1104-1113Google Scholar, 3Gomez-Abellan P. Hernandez-Morante J.J. Lujan J.A. Madrid J.A. Garaulet M. Clock genes are implicated in the human metabolic syndrome.Int J Obes (Lond). 2008; 32: 121-128Google Scholar, 4Srinivasan V. Smits M. Spence W. Lowe A.D. Kayumov L. Pandi-Perumal S.R. et al.Melatonin in mood disorders.World J Biol Psychiatry. 2006; 7: 138-151Google Scholar). The previous two reviews by Reiter et al. (5Reiter R.J. Tan D.X. Galano A. Melatonin and the circadian system: contributions to successful female reproduction.Fertil Steril. 2014; 102: 321-328Abstract Full Text Full Text PDF Scopus (131) Google Scholar) and by Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar) have also described the adverse effects of altered lighting schedules on reproductive function including ovulatory and placental function, and the onset of labor, respectively. Most of the health disorders associated with shiftwork can be attributed to unavoidable chronic sleep deficiency and recurrent circadian rhythm disruption. Numerous physiological functions exhibit a circadian (∼24 hours) profile, and these can be broadly divided into molecular, endocrine, and behavior/activity rhythms. Disruption of circadian rhythms is common in shiftworkers, with exposure to nocturnal lighting being the most important disruptive factor. Shiftwork misaligns physiologic rhythms with respect to each other and to external environmental rhythms such as the 24-hour light/dark cycle. The most common approach to counteract the adverse health effects of light exposure during night shiftwork has been to alter the internal circadian phase of subjects such that the new rhythm matches the altered light/dark cycle during shiftwork. In other words, attempts have been made to invert circadian rhythms by exposure to bright light at night and exposure to darkness during the day. Several studies have shown that combined use of bright light at night and dark goggles that reduce light intensity and short-wavelength light transmission during the day may facilitate circadian adaptation to permanent night shiftwork (7Boivin D.B. Boudreau P. Tremblay G.M. Phototherapy and orange-tinted goggles for night-shift adaptation of police officers on patrol.Chronobiol Int. 2012; 29: 629-640Google Scholar, 8Sasseville A. Hebert M. Using blue-green light at night and blue-blockers during the day to improve adaptation to night work: a pilot study.Prog Neuropsychopharmacol Biol Psychiatry. 2010; 34: 1236-1242Google Scholar). However, an inversion of the circadian rhythm is seldom achieved outside of laboratory conditions, even across successive night shifts and after years of night work experience (9Costa G. Shift work and occupational medicine: an overview.Occup Med (Lond). 2003; 53: 83-88Google Scholar). One of the reasons this simple strategy fails in practice may be unavoidable exposure to bright light in the morning during the home commute after the night shift, or during weekends (10Boivin D.B. Czeisler C.A. Resetting of circadian melatonin and cortisol rhythms in humans by ordinary room light.Neuroreport. 1998; 9: 779-782Google Scholar). We, and others, have shown that selectively removing wavelengths shorter than ∼500 nm from nocturnal illumination prevents melatonin suppression induced by light exposure at night (8Sasseville A. Hebert M. Using blue-green light at night and blue-blockers during the day to improve adaptation to night work: a pilot study.Prog Neuropsychopharmacol Biol Psychiatry. 2010; 34: 1236-1242Google Scholar, 11Kayumov L. Casper R.F. Hawa R.J. Perelman B. Chung S.A. Sokalsky S. et al.Blocking low-wavelength light prevents nocturnal melatonin suppression with no adverse effect on performance during simulated shift work.J Clin Endocrinol Metab. 2005; 90: 2755-2761Google Scholar, 12Sasseville A. Paquet N. Sevigny J. Hebert M. Blue blocker glasses impede the capacity of bright light to suppress melatonin production.J Pineal Res. 2006; 41: 73-78Google Scholar). We have recently demonstrated, in an animal model, that filtering a narrow range of wavelengths (between 450 and 480 nm) from nocturnal lighting can attenuate alterations in hormone secretion (melatonin and corticosterone) and in central and peripheral clock gene (Per2 and Bmal-1) expression (13Rahman S.A. Kollara A. Brown T.J. Casper R.F. Selectively filtering short wavelengths attenuates the disruptive effects of nocturnal light on endocrine and molecular circadian phase markers in rats.Endocrinology. 2008; 149: 6125-6135Google Scholar). We extended these studies to humans in a simulated night shiftwork environment. Thirteen normal volunteers, who were screened to rule out any sleep dysfunction, were kept either in darkness, bright light (fluorescent ∼800 lux), or filtered bright light (fluorescent ∼800 lux while wearing glasses fitted with optical filters to block all wavelengths below 480 nm) for the entire duration of the study between 2000 and 8000 hours. In addition, in a fourth night study, light was filtered using identical glasses fitted with commercially available color-tinted lenses (placebo). Exposure to light at night suppressed the nocturnal rise in melatonin (Fig. 1), increased cortisol secretion, and shifted the expression of the clock genes Per2 and Bmal-1 (14Rahman S.A. Marcu S. Shapiro C.M. Brown T.J. Casper R.F. Spectral modulation attenuates molecular, endocrine and neurobehavioral disruption induced by nocturnal light exposure.Am J Physiol Endocrinol Metab. 2011; 300: E518-E527Google Scholar). Although the placebo filters were ineffective, filtering wavelengths below 480 nm from polychromatic white light was successful in preventing melatonin suppression (Fig. 1), cortisol elevation, and circadian disruption of clock gene expression by light at night (14Rahman S.A. Marcu S. Shapiro C.M. Brown T.J. Casper R.F. Spectral modulation attenuates molecular, endocrine and neurobehavioral disruption induced by nocturnal light exposure.Am J Physiol Endocrinol Metab. 2011; 300: E518-E527Google Scholar). Furthermore, there were no significant differences in alertness, sleepiness, fatigue, or vigilance after restoring normal melatonin secretion using filtered light exposure. One drawback of these lenses is a slight yellow hue that sharpens visual acuity by increasing contrast, but may make recognition of a few colors problematic. We followed this laboratory trial with a field study in nurses working a rapid rotation night/day shift schedule and confirmed the beneficial hormonal effects of filtering out short wavelengths from light at night (15Rahman S.A. Shapiro C.M. Wang F. Ainlay H. Kazmi S. Brown T.J. et al.Effects of filtering visual short wavelengths during noctural shiftwork on sleep and performance.Chronobiol Int. 2013; 30: 951-962Google Scholar). We also demonstrated improved sleep duration and quality by polysomnography (PSG) on nights immediately following night shifts. There was an improvement in mood and cognitive performance toward the end of the night shift with the use of the optical filters as well (15Rahman S.A. Shapiro C.M. Wang F. Ainlay H. Kazmi S. Brown T.J. et al.Effects of filtering visual short wavelengths during noctural shiftwork on sleep and performance.Chronobiol Int. 2013; 30: 951-962Google Scholar). With this new information that disruptions in circadian phase markers can be attenuated or prevented by eliminating short wavelengths from light at night, it may be possible to attenuate circadian misalignment, and the optical filters can be used as a method to improve or prevent many of the adverse medical changes associated with shiftwork. For female shiftworkers, allowing normal melatonin secretion at night might prevent the increased risk of breast cancer, metabolic problems such as insulin resistance, and depression and sleep disturbances. Specifically with regard to this month's View and Reviews focus on reproduction, another speculation is that reproductive function could be improved by using optical filters in women exposed to light at night. For example, the restoration of melatonin rhythms by filtering short-wavelength light could improve follicle development and ovulatory function as suggested by Reiter et al. (5Reiter R.J. Tan D.X. Galano A. Melatonin and the circadian system: contributions to successful female reproduction.Fertil Steril. 2014; 102: 321-328Abstract Full Text Full Text PDF Scopus (131) Google Scholar). If melatonin plays a role in placental function and fetal development, there could also be a beneficial effect on the pregnancy, although future studies are required to investigate these hypotheses. Similarly, the onset of labor is usually nocturnal, likely because of the synergistic effect of melatonin on oxytocin receptors as described by Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar). Their fascinating demonstration that exposure of women in labor to bright light for as little as 1 hour was capable of inhibiting contractions supports the possible synergistic effect of melatonin and oxytocin. To extrapolate these findings clinically, one could hypothesize that when women are admitted to the hospital in labor at night, exposure to overhead lighting could inhibit uterine contractions by suppressing melatonin levels, thus prolonging the time to the second stage of labor. In this situation, we speculate that the use of optical filters that block short-wavelength light could have beneficial effects by preventing the suppression of melatonin and allowing labor to progress normally with maintenance of the quality and strength of contractions and shortening of the latent and active phases of labor. On the other hand, Olcese and Beesley (6Olcese J. Beesley S. The clinical significance of melatonin receptors in the human myometrium.Fertil Steril. 2014; 102: 329-335Abstract Full Text Full Text PDF Scopus (25) Google Scholar) suggest that some women enter premature labor because of the early induction of melatonin receptors in the myometrium. In these women, exposure to light at night, and suppression of melatonin secretion, could have a favorable effect in inhibiting contractions. Taken together, all of the described studies suggest that the invention of the electric light, while enhancing our lives in many ways, may also have deleterious effects on several aspects of human health, including reproductive function. Filtering or removing short wavelengths from light may potentially abrogate these deleterious effects.