Ⅵ Puberty

Somnological Aspects of Puberty

JMAJ 48(3): 114–122, 2005

Kiyohisa TAKAHASHI

President, Aino University

Abstract: The characteristics of during puberty are discussed from the physiological aspect of hormone secretion and from the social aspect of reduced sleep time. Many types of hormones show an increased rate of secretion during sleep at night. Thus, sleep cannot simply be said to represent a stoppage of activities, and rather it comprises another form of ‘activity.’ During puberty, in par- ticular, the secretion of sexual hormones increases during sleep. Sleep is therefore assumed to play a role in promoting the maturation of sexual function. However, in Japan, the amount of sleep time that junior-high school students get has been on the decline. One of the factors contributing to this decline is that students are going to at increasingly later times. Students who go to sleep at late hours at night show a high incidence of problems, such as feeling unwell when they awake in the morning, being unable to consume breakfast, having irregular bowel movements, feeling drowsy during the day, and physically feeling they didn’t get a sufficient amount of sleep at night, as well as other problems. Because the same group tends to show similar symptoms even during summer vacation when the number of hours of sleep increases, it is clear that this is not simply due to reduced sleep time. Accordingly, the increasingly later times at which they go to sleep must be recog- nized as a major problem. Key words: Puberty; Sleep-awake rhythm; Sleep health; Growth hormones; Gonadotropic hormones

Introduction published a report entitled “Proposal regarding the establishment of the scientific field of The theme presented in this paper is focused in Japan and promotion of its on ‘somnological aspects of puberty’ and it study”.1) The aim of this proposal concerning should be noted that the term ‘somnology’ somnology was to integrate the various sleep- itself is considered to be a relatively new one. related studies that are currently conducted in Recently, the Science Council of Japan (SCJ) many different academic fields and to create an

This article is a revised English version of a paper originally published in the Journal of the Japan Medical Association (Vol. 129, No. 10, 2003, pages 1579–1585). The Japanese text is a transcript of a lecture originally aired on December 12, 2002, by the Nihon Shortwave Broadcasting Co., Ltd., in its regular program “Special Course in Medicine”.

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academic system for the science. sively in Japan in 1996 revealed that one out of For the newly proposed field of somnology, five adults in the country suffers from some the areas in which sleep-related studies are forms of .2) Meanwhile, according conducted comprise three major realms. The to one hypothesis, the lifestyle habits of adults first is “sleep science” in which basic studies are formed mostly during puberty. Therefore, are implemented involving molecular biology in order to eliminate the problem of sleep dis- and genetic studies. The second is “sleep medi- orders, people must begin to take care of their cine” which attempts to clinically treat sleep- sleep during puberty. It is also known lessness and . Because dentistry that one pattern of sleep disorder called ‘sleep- and pharmacology are related to this area, this awake rhythm disorder’ begins to appear when field is also called “-dentistry- people are in their mid-teens, or a certain time pharmacology.” And the third is “sleep sociol- from the onset of puberty to the beginning ogy” which attempts to treat social problems of young adulthood.3) In light of the above, related to sleep, such as those regarding the people’s lifestyle behaviors during puberty are so-called ‘night-based society,’ , and very important. accidents resulting from shift work. The above represents the content of the proposal by the 1. Survey studies regarding the sleep habits SCJ in which these three major study fields are of junior-high school students integrated under the main theme of “sleep,” Regarding the sleep problems seen among and based on which an academic system is junior-high school students, a survey was con- structured. The purpose of this proposal is: to ducted recently by a research organization at further promote sleep studies in a way that the National Institute of Mental Health of the transcends each specific field, to apply and National Center of Neurology and Psychiatry, reflect the results of such studies in society, and this survey is discussed herein.4) The orga- to protect the nation from sleep disorders, to nization implemented a survey on the sleep improve people’s overall health, to prevent habits of students at two junior high schools in accidents such as those caused by drowsiness, Okinawa Prefecture during summer vacation. and to eventually increase relevant economic The survey targeted a total of 527 male and effects produced by better sleep habits. female students. The reason summer vacation In this paper, various characteristics observed was selected was because there were no restric- during puberty are listed from the viewpoint of tions regarding what time the students had somnology, and two matters are described in to wake up, in contrast to during the school particular. First, the results of a survey on ‘actual term, and the survey could thus be conducted sleep-related conditions’ are presented which under relatively less restrictive conditions. show that a major problem is occurring in They implemented a questionnaire-type survey terms of the sleep patterns of junior-high which asked what time the students went to school students, a key pubescent age group. bed, what time they got up, the students’ sub- Secondly, the increased rate of hormone secre- jective evaluation of their sleep, how they felt tion as an ‘activity’ during sleep in the vital when they woke up, whether they consumed organs is discussed in terms of the relationship breakfast, their amount of daytime drowsiness, between specific sleep patterns during puberty their level of concentration ability, and others and the secretion of hormones. questions over a period that lasted for about two months. Problems Regarding Sleep Time The results were as follows. The time at which the students went to bed ranged from An epidemiological survey conducted exten- 9:30 pm to 3:00 am, and the percentage of stu-

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Table 1 Comparison among the Sets of Students Grouped according to the Time They Go to Sleep, the Time They Get Up, and the Duration of Their Sleep

Time they went to sleep Time they got up Sleep time Items Delayed Non-delayed Delayed Non-delayed Reduction Normal group group group group group group Feeling unwell when they wake up 37.1 20.5** 35.2 21.7** 26.9 23.4 Irregular consumption of breakfast 51.2 19.7** 57.5 19.5** 30.8 16.2** Irregular bowel movements 33.1 29.3 33.7 29.3 33.1 24.0 Intolerable daytime drowsiness 4.8 2.8 3.8 3.1 6.2 3.1 Physically feeling they didn’t get 60.0 62.1 49.5 64.6** 79.2 61.5** a sufficient amount of sleep Complaints of sleep problems 17.1 10.9† 14.4 11.9 15.3 7.0* ** pϽ0.01 *pϽ0.05 †pϽ0.10 (Cited from Tanaka, H. et al.: Mental Health Research 2000; 46: 65Ð71.)

dents who went to bed after midnight was sleep, waking up too early, , sleep 12.8% for the first-grade students, 19.8% for apnea, difficulty in waking up, and hypnagogic the second-grade students, and 38.6% for the disorder. third-grade students. On the other hand, the The ‘delayed sleep group’ tended to feel times that they woke up ranged from 4:00 am to unwell when they woke up and consumed 3:00 pm and the average was 8:00 am. Their breakfast irregularly, and they manifested wakeup times correlated positively with the many sleep problems such as physically feeling times at which they went to bed, and 7% of all they didn’t get a sufficient amount of sleep at students regularly got a short amount of sleep night and experiencing daytime drowsiness. A lasting six hours or less. Students who went to similar tendency was seen in the ‘reduced bed late woke up at later times with a longer sleep-time group.’ Meanwhile, the ‘delayed amount of sleep time. wakeup group’ who were thought to have A comparison of “sleep health risk” was con- gotten longer hours of sleep also said they felt ducted among three different sets of students: unwell when they woke up and were often 1) Those who went to bed by midnight (‘non- unable to eat breakfast and felt they didn’t get delayed sleep group’) and those who went to a sufficient amount of sleep. The group who bed at the latest times [25%] (‘delayed sleep slept irregularly showed a higher level of sleep group’); 2) those who got up before 9:00 am health risk and were unable to fall asleep easily (‘non-delayed wakeup group’) and those who and could not get up early in the morning, in got up after 9:00 am (‘delayed wakeup group’); comparison with the group who slept regularly. and 3) those who got six or less hours of sleep As mentioned earlier, this survey was carried (‘reduced sleep-time group’) and those who got out during summer vacation when there were six or more hours of sleep (‘normal sleep-time no restrictions in place as to what time the stu- group’). Consequently, the results shown in dents had to wake up. In other words, they Table 1 were obtained. The ‘sleep health risk’ could sleep as much as they wanted. Even comprises a score which results from the inte- under such conditions, differences were still grated evaluation of various factors, including seen regarding the time they went to sleep disorders related to maintaining sleep function, and the regularity of their sleep. Thus, an such as frequent awakening, excessively deep increase in sleep health risk and ‘feeling poorly

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Consuming Feeling unwell when Feeling of (%) no breakfast** (%) they wake up** (%) sleeplessness** 37.0 25.0 22.2 40.0 20.0 14.6 20.0 30.0 23.8 15.0 9.5 15.0 20.0 10.0 10.3 10.0 10.0 5.0 5.0 0.0 0.0 Non-delayed Delayed Non-delayed Delayed Non-delayed Delayed group group group group group group

Physically feeling Excessive Nodding off in class** they didn’t get a sufficient daytime sleepiness** (%) amount of sleep** (%) (%) 90.0 85.0 15.0 13.3 70.0 62.2

80.0 10.0 55.0 47.0 70.9 5.7 70.0 5.0 40.0

60.0 0.0 25.0 Non-delayed Delayed Non-delayed Delayed Non-delayed Delayed group group group group group group Fig. 1 Comparisons between the students who went to sleep at midnight or later (Delayed group) and those who went to sleep before midnight (Non-delayed group) The comparisons regarding ‘mental and physical conditions at daytime’ and ‘not consuming breakfast’ are shown. ␹ 2 test, **pϽ0.01. (Cited from Arakawa, M. et al.: School Health Research 2001; 43: 388Ð398.)

during the daytime’ are assumed to result from Taking these findings into consideration, it lowered sleep quality. In the group who went can be said that going to sleep at later times, to bed at later times at night, there were many irregular sleep habits, and not consuming students who slept and got up at irregular breakfast are associated strongly with a dete- times. rioration of sleep health. Thus, it is important The same research organization also con- for people to acquire regular sleeping and eat- ducted another study which examined sleep ing habits on a routine basis. Students’ sleep health risks of junior-high school students and time is restricted by the time at which they have then compared the level of such risks during to be at school the following morning, and the summer vacation and the school term. In sum- time they must go to bed is almost fixed. It mer vacation, students went to bed and woke is therefore necessary for students to receive up at later times and their sleep health risk was appropriate and adequate instruction regard- significantly higher.5) The students who mani- ing the importance of going to bed at an earlier fested a high level of sleep health risk during time. the school term and during summer vacation tended to have irregular sleep habits and they 2. The effects of -taking went to bed at later times. Moreover, a sub- Another study pointed out that the reason sequent survey conducted which targeted an why students go to sleep at later times was increased number of subjects during the school because they often slept for short periods dur- term confirmed that later times of going to ing the day, i.e. they took .7) According to sleep caused a reduction in the amount of sleep this study, about half of all junior and senior- time and consequently caused a deterioration high school students surveyed said they often in overall sleep health (Fig. 1).6) take naps. Because they take brief naps at

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9.5 Do not take brief naps able for sleep. Take a brief nap once or twice a week Take brief naps three times or 3. Night-shifted lifestyles and reduction of 9 more a week sleep time The “National Time Use Survey” imple- 8.5 mented by the NHK Broadcasting Culture Research Institute every five years since 1969

The degree of irritationThe degree 8 shows clearly that the lifestyles of Japanese people have shifted more and more towards nighttime-focused activities.8) In 1960, about 7.5 22:00 23:00 0:00 1:00 90% of the population went to bed at 11:00 pm, The time they go to sleep yet this figure decreased to around 51% by the Fig. 2 The relationship between taking brief naps and year 2000. Also, in 1960 about 60% of the experiencing irritation during the day people in Japan got up at 6:00am, while in 2000 The junior-high school students were divided into three approx. 60% of people were still asleep at this groups according to how often they take brief naps and their degree of irritation. In all groups, the degree of irri- hour. Although a reduction in sleep time was tation increased when they went to sleep later at night. seen across the board for all age groups, this (Reprinted from Fukuda, K.: Proposal Regarding the Establishment of the Scientific Field of Somnology in tendency was shown most significantly in the Japan and Promotion of Its Study. Japan Science Council, generation aged 16–19 (from the latter half of 2002; pp.69Ð96.) puberty to early young adulthood). Compared with other countries, young people in Japan sleep a shorter amount of hours, and young home after returning from school, the timing of Japanese in the pubescent years (including the naps occurs at a relatively later time during junior-high school students) get 30 minutes less the day, between 5:00–9:00 pm in many cases. sleep each night than their counterparts in These brief naps taken at a later time during America, and one hour and 30 minutes less the day cause the students to go to bed at a sleep than youngsters in European countries.7) later hour of night. And it was found that the The optimal situation is to make sure that later they go to sleep, the stronger feelings of pubescent children, who represent the future irritation they experience during the daytime generation, get a sufficient amount of good- (Fig. 2).7) Besides these findings, it was also quality sleep each night so that they can mature shown that students experience a greater inci- into mentally and physically healthy adults. dence of problems such as anxiety and depres- sion when they go to sleep at later times and Hormonal Secretion during Sleep take frequent naps. Because school starts at a fixed time for The relationship between sleep and endo- junior and senior-high school students, it is crine function is another characteristic that can considered that there are no major individual be discussed regarding puberty. Although vari- differences in the time they get up. Thus, it is ous hormonal secretions increase, one of the assumed that the total sleep time becomes most prominent of these is the growth hor- longer for students who take naps. However, mone. It is known that secretion of this hor- the fact that students who take naps are more mone increases corresponding with the period prone to feeling irritated and have more prob- of deep sleep that occurs at the initial stage of lems indicates that the overall quality of sleep nocturnal sleep.9) On the other hand, its secre- is important and that there are certain hours tion is prevented when a person suffers from during the 24-hour cycle which are more suit- . That is, the growth hormone

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Awake Awake REM Pre-puberty REM First stage of puberty sleep sleep ϳMiddle stage I I II II III III IV Sleep stage IV Sleep stage 10 10 ) ) l 8 l 8 6 6 4 4

LH(mIU/m 2 LH(mIU/m 2 0 0 22 2 6 10 14 18 22 22 2 6 10 14 18 22 Time Time

Awake REM sleep Middle stage of puberty Awake I ϳLatter stage II REM Adulthood III sleep IV

Sleep stage I 18 II III IV 16 Sleep stage 14 14 )

l 12 12 )

10 l 10 8 8

LH(mIU/m 6 6

4 LH(mIU/m 4 2 2 0 0 22 2 6 10 14 18 22 22 2 6 10 14 18 22 Time Time

Fig. 3 24-hour pattern of the secretion of gonadotrophic hormone (LH) for each growth generation The inset of each figure at the upper left shows the sleep pattern. Hormonal secretion in early puberty only increases during sleep. Although the hormones are also secreted during the day in later puberty, the secretion level is higher during sleep. .Boyer, R.M. et al.: J Clin Endocrinol Metab 1976; 43: 1418Ð1421/Yamanaka, HסReprinted from the original) et al.: Clinical Examinations 1996; 30: 831Ð834.)

is secreted during sleep and this is thus the rea- day and night, for example in cases where son why it is said “a child who sleeps well grows people sleep during the daytime and not at well.” Secretion of the growth hormone related night. That is, while the growth hormone is to sleep continues until adulthood or later. This secreted in association with sleep, ACTH has a hormone affects growth and has a function secretion pattern that is associated with time. which synthesizes proteins, and is assumed to Among the hormones which are secreted in play a role in repairing the vital organs at night. association with sleep, there is prolactin pro- Meanwhile, the secretion of adrenocortico- moting the production of breast milk, galactor- tropic hormone (ACTH) decreases during the rhea.10) Moreover, there is also gonadotropin early stages of sleep and then increases during (luteinizing hormone (LH), etc.) which is the latter part. The peak occurs at the time near secreted in association with sleep only during dawn. Unlike the growth hormone, the secre- puberty. The secretion of this hormone begins tion pattern is not changed by the reversal of to increase during pre-puberty and increases

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Awake Normal sleep I II III IV REM sleep

Sleep stage (mIU/ml) 15 12 9 6

Blood LH level 3

Awake Reversed sleep I II III IV REM sleep

Sleep stage (mIU/ml) 15 12 9 6

Blood LH level 3 10 14 18 22 2610 Time Fig. 4 Sleep dependency on the secretion of gonadotrophic hormone (LH) When day and night are reversed, i.e. when people sleep during the daytime (lower section), LH secretion occurs in the daytime, which is not seen usually (upper section). /Kapen, S. et al.: J Clin Endocrinol Metab 1974; 39: 293Ð299סReprinted from the original) Yamanaka, H. et al.: Clinical Examinations 1986; 30: 831Ð834.)

during sleep at night when a person reaches better to say that the reason why people sleep puberty (Figs. 3, 4).11,12) This increase is associ- is so that they can produce hormones. Accord- ated with sleep and the hormone is not secreted ing to recent sleep studies, it has been shown without sleep (it is secreted when people take that the specific sleep pattern called REM naps). In males, the secretion of testosterone sleep is necessary for memory. Thus, sleep is increases in proportion to it (Fig. 5).13) The not a complete stoppage of activities, and fact that the secretion of the gonadotrophic rather it is another condition of ‘activity.’ Such hormone increases during nocturnal sleep recognition is considered especially important only during puberty indicates that sleep is very for puberty. That is, puberty represents an important for ensuring that young mature important growth stage in which sexual matu- sexually. ration is promoted by sleep. It is also shown that the reduction of sleep and sleep quality Conclusion affects the overall quality of a person’s ordi- nary life significantly. It is important that the In this paper, sleep characteristics during whole society including teachers and parents puberty were discussed from the social aspect recognize these matters sufficiently. of reduction of sleep time as well as the aspect of hormone secretion during sleep. Although REFERENCES sleep is often considered a stoppage of activi- ties, it is in fact not, and instead it activates the 1) Japan Science Council: Proposal Regarding secretion of hormones at night. It would be the Establishment of the Scientific Field of

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Awake REM sleep I II III

Sleep stage IV (mIU/ml) 8 Start 6 4

Blood LH level 2 End (ng/100ml) Start 500 400 End 300 200 100 estosterone level T 0 22 2 6 10 14 18 22 Time Fig. 5 24-hour pattern of secretion of gonadotrophic hormone (LH) and testosterone The upper part shows a sleep-course diagram. During sleep, LH and testosterone are secreted at the same phase and with the same pattern. It is assumed that the secretion of testosterone may increase in proportion to LH. .Boyar, R.M. et al.: J Clin Inves 1974; 54: 602Ð619/Yamanaka, HסReprinted from the original) et al.: Clinical Examinations 1986; 30: 831Ð834.)

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177: 1205–1207. 13) Boyar, R.M., Rosenfeld, R.S., Kapen, S. et al.: 11) Boyar, R.M., Wu, R.H., Roffwarg, H. et al.: Human puberty. Simultaneous augmented Human puberty: 24-hour estradiol in pubertal secretion of luteinizing hormone and test- girls. J Clin Endocrinol Metab 1976; 43: 1418– osterone during sleep. J Clin Invest 1974; 54: 1421. 609–618. 12) Kapen, S., Boyar, R.M., Finkelstein, J.W. et al.: 14) Yamanaka, H., Imai, K. and Mashita, T.: Effect of sleep-wake cycle reversal on luteiniz- Circadian rhythms of LH-testosterone and ing hormone secretory pattern in puberty. ACTH-cortisol in males. Clinical Examina- J Clin Endocrinol Metab 1974; 39: 293–299. tions 1983; 30: 831–834. (in Japanese)

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