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Circadian Time of Morning Light Administration and Therapeutic Response in Winter Depression

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Circadian Time of Morning Light Administration and Therapeutic Response in Winter Depression ORIGINAL ARTICLE Circadian Time of Morning Light Administration and Therapeutic Response in Winter Depression Jiuan Su Terman, PhD; Michael Terman, PhD; Ee-Sing Lo, PhD; Thomas B. Cooper, MA Background: We investigated a possible mechanism of advances were larger the earlier the morning light action for the antidepressant response to light—phase ad- (r=0.50). Although depression ratings were similar with vances of the circadian clock—by measuring the onset light at either time of day, response to morning light in- of melatonin secretion before and after light treatment creased with the size of phase advances up to 2.7 hours in the morning or evening. (r=0.44) regardless of baseline phase position, while there was no such correlation for evening light. In an ex- Methods: Plasma melatonin was sampled in 42 pa- panded sample (N=80) with the sleep midpoint used as tients with seasonal affective disorder, in the evening or a reference anchor for circadian time, early morning light overnight while depressed and after 10 to 14 days of light exposure was superior to late morning and to evening therapy (10000 lux for 30 minutes) when symptoms were exposure. reassessed. Conclusion: The antidepressant effect of light is poten- Results: Morning light produced phase advances of the tiated by early-morning administration in circadian time, melatonin rhythm, while evening light produced de- optimally about 8.5 hours after melatonin onset or 2.5 lays, the magnitude depending on the interval between hours after the sleep midpoint. melatonin onset and light exposure, or circadian time (morning, 7.5 to 11 hours; evening, 1.5 to 3 hours). De- lays were larger the later the evening light (r=0.40), while Arch Gen Psychiatry. 2001;58:69-75 HE FIRST controlled clini- many studies have found that a shift to an cal trial of bright light treat- earlier phase position accompanies the an- ment for seasonal affective tidepressant response to morning light5,8,10-12 disorder (SAD)1 demon- or morning plus early evening light,13 a cor- strated a therapeutic effect relation between the size of phase shifts and with daily exposures in the morning and clinical improvement has not been demon- T 14-18 evening. Since then there have been nu- strated, which weakens the argument for merous studies indicating an advantage of a causal effect. morning over evening light exposure in The present study, which used plasma cross-center pooling of data2 and a Co- melatonin onset as the circadian phase chrane meta-analysis.3 Recently, 3 large marker, was designed with 3 questions in clinical trials have further established a mind: (1) Do patients with winter depres- benefit over nonphotic placebo con- sion show contrasting phase shifts under trols,4 the superiority of morning light over morning and evening light therapy? (2) Do evening light exposure,5 or both.6 those who are phase-typed as relatively de- The pathogenesis of SAD and mecha- layed respond preferentially to morning From the Clinical nism of action of light remain uncertain de- light? (3) Is treatment efficacy correlated Chronobiology Program spite numerous investigations.7 A poten- with the direction and magnitude of phase (Drs J. Terman and tial role for abnormal circadian timing shifts? M. Terman), and the gained credence because the effects of light Department of Analytical (including phase shifting and melatonin RESULTS Psychopharmacology (Dr Lo suppression) had been well established in and Mr Cooper), New York 8-10 State Psychiatric Institute, New both humans and animals. Lewy et al pro- TIMING OF MELATONIN York, and the Department of posed that morning light would be effec- SECRETION AND SLEEP Psychiatry (Dr M. Terman), tive because it provides corrective phase ad- Columbia University, vances of delayed circadian rhythms in Total melatonin production in overnight New York. patients with winter depression. Although sessions did not differ under baseline, morn- (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 58, JAN 2001 WWW.ARCHGENPSYCHIATRY.COM 69 ©2001 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 SUBJECTS AND METHODS which they returned home. Nineteen of these subjects com- pleted all 3 assessments; 2 subjects whose baseline ses- SUBJECTS sions were aborted for technical reasons completed only posttreatment assessments; and 12 subjects were sched- Participants included 42 research volunteers aged 21 to 56 uled for and completed only baseline and first-period as- years (mean±SD, 39.2±9.3 years), with 29 women (69%) sessments. Given these variations, we used the maximum and 13 men (31%). Intake evaluations were based on the available sample size for each analysis. Structured Clinical Interview for DSM-III-R,19 adminis- Blood samples (4 mL) were obtained while subjects tered by trained research staff. Diagnoses20—all with sea- were seated or resting in bed, using an indwelling venous sonal pattern, winter type—were major depressive disor- catheter in the forearm. Ambient illumination was 1 to 5 der, recurrent (code 296.3) in 29 subjects (69%), and bipolar lux provided by a 15-watt shaded incandescent reading lamp. disorder not otherwise specified (code 296.7) in 13 (31%). Subjects commenced dim light exposure at least 1 hour be- Candidates with comorbid Axis I disorders or recent his- fore the first sample was collected. Illumination remained tory of a suicide attempt were excluded. Subjects were part constant across the sampling sessions except during sleep of a larger group that underwent clinical trials of light when the light was extinguished. therapy6 but were also available for evening or overnight Blood was centrifuged and plasma was separated and laboratory sessions during which blood was sampled for frozen for further analysis. The plasma was subjected to a melatonin concentration. An expanded analysis (N=80) in- direct radioimmunoassay based on an antiserum obtained cluded 38 additional subjects from the complete group6 who from the University of Surrey, Guildford, England. The as- provided sleep logs but not melatonin data. say was cross-validated against gas chromatography/mass spectrometry in collaboration with A. J. Lewy, MD, PhD PROCEDURE (Oregon Health Sciences University, Portland). The com- parison yielded a high correlation (r=0.95; slope, 1.02; in- Details of treatment have been previously described.6 Within tercept, 5.7 pg/mL), and we achieved a lower detectable limit a crossover design, 21 subjects first received morning light of 2.5 pg/mL. In 8 consecutive analytical runs with 3 qual- and then evening light (M1E2), and 21 received treatment ity control levels (22, 33, and 93 pg/mL), the within- and in the opposite order (E1M2). Transitions were immedi- between-run relative SD percentages were 10.4 and 14.6, ate, without withdrawals. After a minimum 2-week base- 12.9 and 11.8, and 3.9 and 4.5, respectively. line interval that verified a current depressive episode, sub- jects received 10 to 14 days of treatment in both periods, STATISTICAL ANALYSIS 30 minutes per day. Subjects were instructed to maintain consistent bedtimes and wake-up times throughout the Rating scale scores were analyzed as raw data and in terms study, according to their habitual schedule. They used the of the percentage change from baseline. Univariate and mul- lights at home either soon after awakening (6:32 AM ±56 tivariate analyses of variance and covariance were used to minutes) or approximately 2 hours before bedtime (9:30 detect group and group 3 period interactions and the in- PM ± 64 minutes). The lighting device provided 10000 lux, fluence of baseline regressors. Linear regression, includ- 2700°K fluorescent illumination through a 28361-cm dif- ing forward stepwise multiple regression (F to enter, 4.0; fusing screen. Raters who were blinded to the treatment to remove, 3.996) and the correlation coefficient, r, were administered the 29-item Structured Interview Guide for the used to measure the relationship between continuous vari- Hamilton Depression Rating Scale–Seasonal Affective Disor- ables. Group means were compared by t tests and categori- der Version (SIGH-SAD)21 at baseline and after both treat- cal differences by the x2 test. For all statistical tests, an a ment periods, on the same days melatonin was sampled. level of .05 (2-tailed) served as the criterion for significant Melatonin was sampled at 30-minute intervals in 2 pro- differences. tocols. Nine subjects underwent 15-hour overnight ses- To test a set of correlations between melatonin phase sions beginning approximately 4 hours before their ha- anchor points across baseline, morning light, and evening bitual sleep onset. Eight of these subjects completed 3 light samples in overnight sessions, the significance of the assessments, at baseline and after both treatment periods, observed value was determined by reference to a random while the ninth declined reassessment after baseline. Thirty- probability distribution of correlations for all 8 permuta- three subjects underwent 5-hour evening sessions after tions of subject pairing, keeping conditions matched. ing light, and evening light conditions (grand mean±SD, time of melatonin synthesis offset (SynOff) estimated by 855±588 pg.30min/mL; F2,14=1.92, P=.18), though there the last high-amplitude data point preceding the steep early 22 were significant interindividual differences (F7,14=54.22, morning decline. The correlation between DLMO and Syn- P=.001). The secretion patterns were similar in shape Off was high (r=0.64, n=23, P=.02 by randomization test; (Figure 1). Melatonin levels began to rise between 8 PM data were excluded in 1 case with an atypical secretion and 10 PM, reaching maximum concentration between 1 pattern). The 2 measures indicated similar bidirectional AM and 4 AM, and returning to daytime levels between 8:30 phase shifts (DLMO vs SynOff for morning light, 1.51±0.87 AM and 10 AM.
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