Sleep. 18(10):895-900 © 1995 American Sleep Disorders Association and Sleep Research Society Environment and Sleep Does a Subtropical Climate Imply a Seasonal Rhythm in REM Sleep? J.J .M. Askenasy and R. Goldstein Sleep Medicine Institute, Sheba Medical Center, Tel Hashomer, Israel Summary: The present study was performed on 615 male subjects referred to the Sleep Medicine Center at Tel Hashomer, Israel, and polysomnographically recorded for a single night between January I, 1990 and December 31, 1993. The study suggests the existence of a circannual rhythm of rapid eye movement (REM) sleep time with an acrophase during December-January and a nadir during July-September (single cosinor analysis: mesor = 49.7 ± 0.9, amplitude = 5.9 ± 1.2, p < 0.001). Both REM sleep time and REM sleep percentage were higher and REM sleep latency shorter during winter and spring than during summer and fall. No dependence of the seasonal REM sleep time rhythm upon age, apnea-hypopnea index or diagnosis type was detected. These data support, for a subtropical climate, results previously obtained in a temperate climate. It is possible that external temperature may be the principal factor influencing the phenomenon. Key Words: REM sleep-Seasonal variation-Circannual rhythm-Male subjects-Subtropical climate. Numerous experimental studies on the interrelationship between sleep architecture and climate have shown that significant changes in rapid eye movement (REM) sleep and slow wave sleep (SWS) parallel changes in the external temperature (1-6) and that the nonrapid eye movement (NREM)/REM ratio depends on the peripheral thermal state (7). Some studies suggest that exposure to cold induces an increase in REM sleep (8,9), whereas a rise in temperature increases SWS and delays REM sleep (5,6,8). However, several studies dealing directly with human sleep and external temperature contradict these findings; thus there is a diminished REM in polar conditions (3) and an increased REM in a subsaharan climate (4). Studies of seasonal sleep architecture rhythms (1,2,9), which are correlated only indirectly to temperature, are more common. Because the most conspicuous aspect of external temperature is its seasonal rhythm, all the studies relating sleep to seasonal rhythms assume that such rhythms are dependent on the external temperature. Weitzman et al. (10) did not find any significant season-dependent changes in sleep architecture. A more recent study, however, described a significant Accepted for publication June 1995. Address correspondence and reprint requests to Dr. J. J. M. Askenasy, Sleep Medicine Institute, Building 16, Sheba Medical Center, Tel Hashomer, 52621, Israel. increase in REM sleep and a parallel decrease in SWS during winter as compared with summer in a temperate climate (2). In this longitudinal study, performed on 10 healthy young male subjects, Honma et al. described seasonal variations in the timing of sleep and mean body temperature (2). They concluded that the phaseangle difference of the rectal temperature rhythm and sleep varied seasonally. We hypothesized that if this conclusion were well founded, a transverse analysis of sleep performed on a large population over four consecutive years and during each of the seasons in our subtropical climate might provide evidence of such a sleep variability. Our expectation was that if a sleep variable had a seasonal rhythm, its interseasonal variability would exceed interindividual variability. A 4-year transverse study was therefore carried out on a large number of patients, each one undergoing a polysomnographic (PSG) examination for I night. The seasonal variations in sleep architecture in male subjects undergoing recordings in a sleep disorders center are presented here. It should be noted that the climate oflsrael is a mixture of two climatic types, "desert" and "rainy", consisting essentially of a long summer (hot and dry), a shorter winter (cold and wet), short springs (warm and dry) and short autumns (mild and dry). 895 J. J. M. ASKENASY AND R. GOLDSTEIN 896 TABLE 1. Main characteristics of the male population investigated over four consecutive years (1990-1993), by season Population characteristics Winter Mean 47.1 ± 14.3 ± SO 31.1% Disease typc-% SAS (103) (number of ED 38.1% cases) (91) Other 40.0% ( 18) Total number of cases 212 Age Spring Summer Fan Total Test p 46.2 ± 15.1 46.9 ± 14.1 47.7 ± 16.2 46.8 ± 14.9 ANOYA 0.89 (NS) 13.2% (57) 20.5% (49) 22.2% 36.3% (120) 24.6% (71) 20.0% (9) 190 15.4% (51 ) 25.5% (61) 17.8% (8) 97 331 F(611,3) (10) 116 =8 239 45 Multiple chi-square test NS 0.10 (NS) 615 SO = standard deviation; NS = not significant; SAS = sleep apnea syndrome; ED = erectile dysfunction. METHODS Subjects Only males were included in the present study. This was because the large majority of patients referred were men (all those with erectile problems, and most of those with suspected sleep apnea), and the small number of women available would have introduced further complications such as menstruation-dependent changes in sleep pattern (11). Our study population therefore consisted of 615 male subjects. The few who were on medication when they were referred to us were told to stop taking it for 8 days before PSG recording. Each subject was polysomnographically recorded for 1 night between January 1, 1990 and December 31, 1993 in the sleep laboratories of the Sleep Medicine Institute at Sheba Medical Center. The recordings were carried out under stable indoor temperature conditions of 18°-20°C. The mean age of the subjects was 46.8 ± 4.9 years (range 2-88 years). There were no statistically significant differences in age in relation to season. The subjects were referred as possibly suffering from sleeprelated breathing disorders (sleep apnea syndrome; SAS) (n = 331), erectile dysfunction (ED) (n = 239) or other problems (n = 45). There was no statistically significant difference in disease distribution in relation to season (Table 1). Equipment and specific methods A single-night PSG was performed by means of a Nikon-Kohden Neurofax polygraph with 18 channels. The full recording comprised three channels for electrooculography (EOG), two channels for electroencephalography (EEG), two channels for electromyography (EMG; submental and right tibialis anterior muscles) and one channel for electrocardiography (ECG), oxygen saturation, nasal air flow and chest and abdominal respiratory movement transducers, respectively. The sleep stages were scored according to the criteria of Rechtschaffen and Kales (12). Sleep, Vol. 18, No. 10, 1995 The following sleep parameters were investigated: 1) Expressed in minutes: time in bed, total sleep time, sleep latency, REM sleep latency, stage I, stage II, stages III-IV ofNREM sleep, REM sleep, longest awakening and longest sleep period; 2) Expressed numerically: REM periods, num ber of arousals, arousals longer than 5 minutes, movement periods and stage transitions; 3) Expressed in percentages (out of total sleep time or from total recording time): stage I, stage II and stages III-IV of NREM sleep, total NREM sleep and REM sleep; 4) Expressed as indices: sleep efficiency, apneahypopnea index (AHI) and O 2 desaturation. Statistics The data were statistically analyzed with EPI Info Version 5 software. Because there were no statistically significant differences in sleep with regard to year, the data for all 4 years were summarized and analyzed together in relation to season. The seasonal sleep variables represent the means of all the daily values obtained during the same season (winter, November 15March 15; spring, March IS-May 15; summer, May IS-October 1; fall, October I-November 15) during all 4 years together, so that the variance of these means represents the seasonal interindividual variability. The seasonal changes of numerical values were evaluated by analysis of variance (ANOV A) at a confidence limit of at least I %. The seasonal changes in paradoxical sleep duration (REM sleep time = RST) according to age group or to the AHI were estimated by multiple analysis of variance (MANOVA) at a confidence limit ofat least I %. Where significant differences were found, the Newman-Keuls multiple comparison test (NKmct) was used, at a significance level of at least I%. The percentage values were analyzed by a multiple chisquare test. Additionally, the monthly values (the cumulative values of all days from the same month from all 4 years) of the sleep variables underwent a separate analysis for a circannual rhythm, using the mean cosinor 897 SEASONAL RHYTHM OF REM SLEEP TABLE 2. Sleep measures, according to season, in male subjects investigated over four consecutive years (1990-1993) ANOYA Sleep measures Winter Sleep continuity measures Total recording time (TRT) (minutes) Total sleep time (TST) (minutes) Sleep latency (minutes) Number of movements N urn ber of arousals Number of awakenings longer than 5 minutes Longest sleep (minutes) Longest awakening (minutes) Sleep efficiency (TST/TRT x 100) NREM sleep measures Stage I time (SI) (minutes) Stage 2 time (S2) (minutes) Stage delta (3 + 4) (SWS) (minutes) Stage I percent (SI/TST x 100) Stage 2 percent (S2/TST x 100) Stage delta percent (SWS/TST x 100) Total NREM percent (SI + S2 + SWS)/TT x 100 REM sleep measures REM latency (minutes) REM time (RT) (minutes) REM percent (RT/TT x 100) Number of REM periods 352.2 ± 54.2 299.6 12.9 7.2 12.1 ± ± ± ± 76.3 16.8 7.4 7.9 Spring 363.3 ± 65.7 306.4 10.6 8.7 13.4 ± ± ± ± 68.5 11.5 6.9 9.9 F(614,3) = P 366.5 ± 50.7 2.44 0.88 (NS) ± ± ± ± 71.8 13.4 6.3 6.4 3.02 1.41 1.12 1.36 0.06 0.24 0.34 0.20 Summer Fall 364.5 ± 53.6 301.9 10.6 8.4 13.8 ± ± ± ± 50.6 13.0 7.5 7.7 300.1 10.7 7.3 13.1 (NS) (NS) (NS) (NS) 2.2 ± 2.0 110.3 ± 68.6 21.9 ± 19.7 2.0 ± 1.9 116.4 ± 64.8 24.3 ± 19.5 2.1 ± 1.7 112.1 ± 63.8 22.7 ± 20.0 1.2 ± 2.1 109.4 ± 64.2 25.7 ± 20.1 0.20 2.12 0.26 0.89 (NS) 0.10 (NS) 0.86 (NS) 81.7 ± 16.5 84.2 ± 12.6 85.3 ± 16.3 84.6 ± 16.6 0.75 0.53 (NS) 29.3 ± 26.9 168.3 ± 59.8 30.3 ± 25.4 172.1 ± 61.6 28.4 ± 22.3 172.4 ± 54.3 30.7 ± 72.7 171.2 ± 59.9 1.7 1.8 0.17 (NS) 0.16 (NS) 45.6 ± 21.7 50.0 ± 37.1 51.8 ± 41.7 48.9 ± 37.2 1.5 0.22 (NS) 9.8 ± 9.1 9.9 ± 8.2 9.4 ± 7.8 10.2 ± 9.2 2.0 0.12 (NS) 56.2 ± 14.8 55.2 ± 14.1 57.1 ± 13.6 57.0 ± 14.6 1.2 0.32 (NS) 15.2 ± 9.6 16.3 ± 12.6 17.2 ± 11.5 16.3 ± 11.5 1.6 0.18 (NS) 81.2 ± 13.6 82.4 ± 13.3 83.7 ± 14.4 85.6 ± 13.9 2.1 0.09 (NS) 109.6 54.4 15.3 3.2 ± ± ± ± 52.2 25.3 6.5 1.3 111.8 52.6 14.1 3.1 ± ± ± ± 63.0 23.7 6.3 1.3 124.6 46.3 12.9 3.1 ± ± ± ± 71.7 29.6 5.7 1.3 99.8 41.5 13.5 3.0 ± ± ± ± 62.7 30.2 6.7 1.3 4.12 4.14 5.1 0.9 <0.007 <0.007 <0.003 0.81 (NS) Bold values represent the minimal values, statistically significant differing from non-bold values (Newman-Keuls multiple comparison test at a significance level of at least 1%). method. The analysis, which consisted of a single cosinor for all 4 years together, with a period of 365.25 days, made possible rhythm detection at a significance level of at least 5%. RESULTS Of all the sleep variables analyzed, only the REM sleep measures displayed significant seasonal differences (Table 2). Both RST and REM sleep percentages were significantly lower during summer and fall than during winter and spring (Table 2). To the contrary, in comparison with spring and summer, REM sleep latency significantly decreased during winter and fall (Table 2). No significant seasonal changes in sleep-related breathing measures (respiration rate, AHI and O 2 desaturation) were detected (Table 3). The fact that the MANOY A test, performed for a seasonal RST pattern according to age groupings, revealed both significant seasonal and significant agerelated differences, whereas the age/season interaction was not statistically significant, demonstrates that the seasonal rhythm of RST is not age related (Table 4). Not only did the AHI not display a significant seasonal pattern (Table 3), but analysis of the seasonal TABLE 3. Sleep-related breathing measures, in male subjects investigated over four consecutive years (1990-1993), by season ANOYA Sleep-related breathing measures (± SD) Winter Spring Summer Fall F(611,3) p Respiration rate Apnea-hypopnea index (AHI) O2 desaturation (%) 15.4 ± 3.4 20.2 ± 36.8 11.8 ± 7.8 16.2 ± 3.3 24.8 ± 36.6 10.7 ± 7.7 16.1 ± 3.4 23.8 ± 33.7 11.1 ± 8.3 16.0 ± 3.1 29.8 ± 35.1 11.3 ± 10.4 0.65 0.45 0.07 0.59 (NS) 0.72 (NS) 0.97 (NS) Sleep, Vol. 18, No. 10, 1995 l J. J. M. ASKENASY AND R. GOLDSTEIN 898 TABLE 4. Mean REM sleep time (RST) in male subjects investigated over four consecutive years (1990-1993), by season and age group (± SD) Age group (years) 21-40 <20 Season 41-60 >60 42.5 ± 21.2 (40) 51.3 ± 24.7 (119) 56.0 ± 26.4 (44) 67.8 ± 37.3 (9) Winter 41.5 ± 21.8 (21) 51.2 ± 22.3 (62) 60.6 ± 31.2 (8) 56.9 ± 23.7 (25) Spring 45.2 ± 20.5 (99) 42.3 ± 19.4 (50) 42.0 ± 17.0 (35) 55.5 ± 31.1 (6) Summer 40.5 ± 21.7 (17) 47.0 ± 23.4 (54) 35.0 ± 26.4 (22) 50.3 ± 31.7 (4) Fall Numbers in parentheses represent numbers of subjects. MANOVA: F(599,3) = 4.39, p < 0.001 for season factor; NKmc test p = 0.01, Winter = Spring> Summer = Fall, F(599,3) = 3.51, p < 0.001 for age factor, NKmc test p = 0.01 «20) > (21-40) = (41-60) > (>61), F(599,9) = 0.23, NS for season-age interaction. changes in RST according to AHI values produced evidence that these changes were not dependent upon the AHI index (Table 5). REM sleep time (RST) values were significantly higher in subjects with SAS and ED than in subjects with other diagnoses, but because no significant diagnosis/season interaction was detected it can be stated that diagnosis did not affect the seasonal pattern of RST (Table 6). When we analyzed the data not on a seasonal but on a monthly basis, cosinor analysis confirmed a circannual rhythm only for RST. Between January 1, 1990 and December 31, 1993, the monthly mean variations of RST displayed a circannual rhythm whose acrophase was during December and January and nadir during July, August and September (Fig. 1). The mean cosinor analysis showed that this rhythm was statistically significant (mesor = 49.7 ± 7.0; amplitude = 5.9 ± 1.2; phase = -6 ± 11; p < 0.001). Of interest is the fact that, as an exception to this general pattern, there was a sharp RST decrease during March (Fig. 1), when a transitory increase of the external temperature is felt in the Israeli climate as a result of the hamsin (a very hot and dry desert wind). DISCUSSION The present results show that, at least in male subjects referred to a sleep disorders center and under the subtropical climatic conditions of Israel, REM sleep duration or time (RST) displays significant seasonal differences, with high values during the winter and spring and low values during summer and fall. The RST also displays a circannual rhythm that reaches its maximum in December and January and its minimum from July to September. Because our study was carried out for one single night on a large population of different subjects, the present results can be interpreted as showing that there is a general tendency for the interseasonal differences of RST to exceed the interindividual differences. The fact that in a subtropical climate both RST and REM sleep percentages are high during winter and low during summer, whereas REM sleep latency displays an inverse pattern, provides evidence for a winter increase (or a summer decrease) in REM sleep pressure, completely confirming results previously obtained in a temperate climate (1,2). Factors known to affect REM sleep, such as age (13), AHI (14) or type of diagnosis (15), did not significantly influence the seasonal pattern of REM sleep that we have noted, and sleep-related breathing disorders did not display any significant seasonal rhythm. These findings strengthen the supposition that REM sleep displays a season-dependent rhythm and support the idea that, apart from all factors that could possibly interfere with REM sleep, this rhythm is a general characteristic of male subjects. (Our study, as stated, excluded women.) It is evident that none of these factors could of itself induce a different sleep structure at different times of the year, because the various presenting problems and ranges in age and AHI were equally dis- TABLE 5. Mean REM sleep time (RST) (± SD) in male subjects investigated over four consecutive years (1990-1993), by season and age group Apnea-hypopnea (AHI) group Season Winter Spring Summer Fall <10 51.0 55.5 46.0 39.0 ± ± ± ± 23.6 25.3 20.5 21.7 10-20 (105) (63) (91) (54) 20-40 >40 55.4 ± 25.3 (31) 56.0 ± 25.8 (40) 54.3 ± 29.2 (36) 51.6 ± 23.5 (19) 57.6 ± 21.7 (21) 45.6 ± 20.7 (13) 50.1 ± 22.8 (32) 46.3 ± 16.5 (31) 42.6 ± 16.3 (36) 45.5 ± 22.8 (8) 41.0 ± 22.0 (19) 40.6 ± 19.7 (16) Numbers in parentheses represent numbers of subjects. MANOV A: F(599,3) = 6.37, p < 0.001, for season factor; NKme test p = 0.01, Winter = Spring> Summer = Fall, F(599,3) = 0.22, NS for AHI group factor, F(599,9) = 0.43, NS for season-NHI interaction. Sleep, Vol. 18, No. 10, 1995 899 SEASONAL RHYTHM OF REM SLEEP CIRCANNUAL RHYTHM OF RST (Data lire cum ulatod for 1990·1993) Q (/) -!.. + :E =: ~ 52 (/) It 48 2 FIG. 1. 3 Circannual rhythm of RST. RST 4 = 5 6 7 MONTHS 8 10 11 12 REM sleep time (duration). tributed throughout the seasons, and the peculiar relationship between season and REM sleep cannot possibly be explained in terms of individual age or pathology. The present data about RST are apparently in divergence with those from previous studies performed in extreme climatic conditions, in which it was found that RST diminishes in a polar climate (4) and increases in subsaharan conditions (5). This discrepancy may be explained in one of two ways. Studies (4) and (5) may provide evidence of the stressful effect of extreme temperature itself rather than of a true seasondependent rhythm; or we may suggest that because the weather in Israel is mainly warm for 10 months ofthe year, people are not accustomed to the cold conditions of winter and therefore display a marked response to them during the months of December and January. Because the temperature within the sleep laboratory was constant throughout the year, the response is clearly not sparked off by a chance coolness for a single night. Our transverse study confirms the increase of REM duration in winter that has been observed in a longitudinal study performed in a temperate climate (2), as well as the increase in REM sleep observed after exposure to cold air (8,9). The entrainer mechanisms of the seasonal rhythm of REM sleep are unknown. However, from the factors known to be possible REM sleep synchronizers, only two can be relevant here: external temperature (2) and day length in relation to light intensity (16). The fact that the occurrence of REM sleep is related to a decrease in core body temperature (7) attests to a possible involvement of temperature in synchronizing REM sleep, as has been suggested in TABLE 6. Mean REM sleep time (RST) (± SD) in male subjects investigated over four consecutive years (1990-1993), by season and diagnosis type Season Sleep apnea syndrome (SAS) Erectile dysfunctions (ED) Other diseases (OTH) 53.0 ± 26.8 (I8) 48.5 ± 21.8 (91) 61.8 ± 26.6 (!O3) Winter 47.2 ± 23.8 (49) 54.2 ± 27.3 (10) 56.4 ± 23.2 (57) Spring 38.9 ± 17.9 (61) 51.6 ± 22.4 (9) 48.5 ± 21.2 (120) Summer 33.9 ± 21.5 (38) 42.5 ± 29.7 (8) 48.0 ± 26.5 (51) Fall Numbers in parentheses represent numbers of SUbjects. MANOYA: F(603,3) = 4.96, p < 0.001 for season factor; NKmc test p = 0.01, Winter = Spring> Summer = Fall, F(603,2) = 6.89, p < 0.001 for diagnosis type factor, NKmc test p = 0.0 I, SAS = OTH > ED, F(603,6) = 0.61, NS for season-diagnosis interaction. Sleep, Vol. 18, No. 10. 1995 J. J. M. ASKENASY AND R. GOLDSTEIN 900 connection with the regulation of the NREM/REM ratio (lO). The sharp decrease in RST observed during March in Israel, when there is a transitory increase in external temperature but the days change very little in length, strengthens the suggestion that an increase in external temperature is immediately followed by a decrease in REM sleep. However, we are also inclined to believe that day length in relation to light intensity may well play an important role in RST seasonal variations. 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