Chronotype and its association with lifestyle, health-related quality of life and academic performance among Japanese nursing students: A cross-sectional study

Background: Generally, nursing university students struggle with academic work, that consequently bring about delayed bed time, insucient sleep and worsened daytime functioning. The purpose of the present study is to clarify chronotype and its association with lifestyle, health-related quality of life and academic performance among nursing students. Methods: Self-reported questionnaires were distributed to undergraduate nursing students at six universities. Chronotype was assessed using the morningness-eveningness questionnaire. The generalized linear mixed effect model was utilized to identify the related factors with evening type among female nursing students (n = 447). Results: About 18% of Japanese female nursing students were identied as evening type. Evening type was associated with living alone, part-time job and club activity. Sleep duration on weekdays was shorter, meal time duration was the shortest, and the percentages of students who skipped meals and those who gained body weight were higher in the evening type than in the morning type and intermediate type. Mental health-related quality of life was lower in the intermediate type and evening type than in the morning type, while there was no difference in physical health-related quality of life among chronotype groups. The percentages of the nursing students who have experienced absence, tardiness, falling asleep during class and/or interference with academic achievement were higher in the evening type than in other chronotypes. Conclusions: Education of sleep hygiene and a healthy lifestyle to prevent late sleep-wake rhythm would contribute to improve nursing students’ health-related quality of life / academic performance.


Background
Sleep is important for maintaining and enhancing one's health. Sleep patterns and sleep problems change along with the life-stage. University students are likely to have late chronotype due to their agedependent delayed endogenous circadian clock(1), school work, extracurricular activities, club activities, or part-time jobs. Nevertheless, they are forced to wake up early controlled by the social clocks (e.g., earlymorning classes or early-morning practice in club activities). Therefore, late chronotype and resulting insu cient sleep are typical sleep problems in this age group. Previous studies have reported that these sleep problems are negatively associated with mental health (2), health-related quality of life (3,4), and academic performance (5,6) in the young population.
Sleep-related problems are not rare in nursing students: 9-12% have di culty initiating sleep, 8-11% have di culty maintaining sleep, and 8-9% have early morning awakening (7,8). Furthermore, the prevalence of insomnia, sleep disturbance, or poor sleep ranges from 19 to 56% (7)(8)(9). Average sleep duration in nursing students varies among countries: 7 hours in Turkey(10) and 5 hours in Philippines(11),with regional differences in sleep duration among university students in general (12). The percentage of nursing students with short sleep duration was 34-60% (< 7 hours)(7, 13) and 13% (< 6 hours)(9); 11-35% of them had daytime sleepiness (14)(15)(16). More than half (59%) of the nursing students took a nap for longer than 30 minutes (7). Taken together, more than a few nursing students may experience insu cient sleep. Furthermore, the previous studies reported that insu cient sleep worsened mental health (17) and health-related quality of life (11), that daytime sleepiness interfered with academic achievement(18), and that subjective poor sleep quality was associated with both physical and mental health (19,20) in nursing students. Because nursing students have more stress, anxiety, sleep disturbance, and stress-related illness than non-nursing students (21,22), there are a few studies which recommend stress coping strategies as an approach to address sleep problems (19,23). However, no studies have focused on age-dependent biological rhythm and chronotype among nursing students.
Chronotype, the tendency towards morningness or eveningness underlying the circadian system, is in uenced by age, gender(1), genetics (24), and external environment/circumstances including light exposure (25) and sociocultural conditions(26). Late chronotype is often accompanied by unique eating behaviors (e.g., breakfast skipping, evening energy intake) (27,28), which result in metabolic disorders including obesity and diabetes (29,30). In addition, late chronotype is associated with poor mental health (31,32) and poor academic achievement in university students (33). Generally, nursing university students struggle with academic work (e.g., reports, studying for registered nurse's licensure exams, graduation research), that consequently bring about delayed bed time, insu cient sleep and worsened daytime functioning. According to the previous study, the amount of academic work was speci ed as a stressor in nursing students (34). However, no studies have assessed nursing students' sleep and daily functioning considering their chronotype.
The purpose of the present study is to clarify chronotype and its association with lifestyle, health-related quality of life and academic performance among nursing students. Building healthy lifestyles during their school days may contribute to improving not only their physical/mental health but also the quality of medical services (e.g., prevention of medical accidents, lowering the turnover rate of nurses) in the future.

Participants and data collection
This cross-sectional study was conducted at six universities with nursing courses in Japan between June 2018 and October 2019. Except for a university in the Tohoku region, a northern area of Japan (n = 57), all the universities were located in the Kanto region (i.e. Tokyo, Kanagawa, Chiba). Self-reported questionnaires were distributed to undergraduate nursing students during the term of normal classes, not in the practical training period. The questionnaires were collected by means of a collection box or envelope so that answerers could not be identi ed, in accordance with the administrative regulation of the ethical approval committee in each university. We received 519 questionnaires from eligible students with a response rate of 48.4%, of which 34 of the respondents were male (7%) and 485 were female (93%). Because the number of male students is small and their chronotype differs from female students, we analyzed only the data obtained from female nursing students. Thirty-eight respondents were excluded from subsequent analyses because their chronotype could not be determined due to missing data. Finally, 447 valid data were used for analyses in the present study.

Measures
The questionnaire was written in Japanese and consisted of the following items.
1. Characteristics of nursing students and lifestyle/social activities Students were required to answer questions on age, sex, grade, starting and closing time of class, whether they were living alone or not, commute time, exercise habits per week (≥ 4 days /2-3 days/ ≤ 1 day/ none), duration of habitual exercise, start time of exercise, part-time job, part-time job after 10 p.m, starting and closing time of part-time job, club activity, and starting and closing time of club activity.
Data on sleep pattern included information on sleep duration, bedtime, awakening time on weekdays and on weekends. The Japanese version of Epworth Sleepiness Scale (35,36) was used to assess the level of daytime sleepiness. The total sum score ranges from 0 to 24, and ≥ 11 is regarded as having excessive daytime sleepiness. Sleep quality was assessed with the Japanese version of Athens Insomnia Scale(37, 38), which indicates possible insomnia when one has a score above ve out of the total score. In order to assess sleep-related symptoms, the self-report questionnaire included questions on di culty initiating sleep, di culty maintaining sleep, early morning awakening, and/or di culty awakening.
Information regarding eating patterns included meal time, duration of meal, skipping meals, and frequency of skipping meals at breakfast, lunch and dinner. In addition, students were required to answer questions on body weight gain after entering the university. Body mass index was calculated by selfreported height and weight.

Chronotype
To assess chronotype, the Japanese version of Morningness-Eveningness Questionnaire (39,40) was used. This questionnaire consists of 19 items, and a total score below 42 is de ned as evening type, 42-58 as intermediate type, and above 58 as morning type. The questionnaire included questions on frequency of absence, tardiness, and falling asleep during class (often/sometimes/none) and interference with academic achievement (yes/no). Frequency was converted into a binary outcome (0: none, 1: often/sometimes).

Statistical analyses
Representative values were shown as mean ± standard deviation. Kruskal-Wallis tests and Chi-square tests followed by residual analyses were performed for continuous variables and categorical variables, respectively. To identify the related factors with chronotype, the generalized linear mixed effect model was used. In the model, explanatory variables; age, living alone, start and closing time of class, commuting time, excise habit, part-time job and club activity were set as xed effect, and university and grade were set as random effect. In the analysis of generalized linear mixed effect model, the degree of association was represented as adjusted odds ratio and 95% con dence interval. In these analyses, complete-case analysis was performed, but no imputation for missing data was performed. The signi cance level was de ned as p < 0.05. Generalized linear mixed effect model was analyzed using R statistical software version 3.5.1 (R Core Team, Vienna, Austria). "lme4" package (43), and other analysis were performed by IBM SPSS Statistics 25 (IBM Corporation, Armonk, USA).

Ethics
Ethical approval for this survey was granted by the Ethical Committee of the Institute of Neuropsychiatry (No.162). All the subjects participated on a voluntary basis and responses were treated anonymously.
Written informed consent was obtained from the participants.

Chronotype and lifestyle/social activities in nursing students
The number of evening type individuals was 80 (17.9%), while those of morning type and intermediate type were 48 (10.7%) and 319(71.4%), respectively.
Characteristics of nursing students and lifestyle/social activities for each chronotype were shown in Table 1. Students ranged in age from 18 to 27, and there was no difference in age among the three chronotype groups. Among the students with evening type, the percentages of the students who lived alone, those who had part-time job, or those who engaged in part-time job after 10 p.m were higher, and the percentage of the students who had an excise habit and/or club activity was lower than that of the morning type and intermediate type. Frequency of part-time job was lower, and starting / closing time of part-time job was earlier in the morning type than in the intermediate type and evening type. In the generalized linear mixed effect model analysis, evening type was associated with living alone (adjusted odds ratio: 2.6, 95% con dence interval: 1.2-5.5), part-time job (adjusted odds ratio: 3.5, 95% con dence interval: 1.3-9.3) and club activity (adjusted odds ratio: 0.3. 95% con dence interval: 0.2-0.7) ( Table 2).

Chronotype and sleep pattern
Sleep patterns in each chronotype were shown in Table 3. Bedtime and wake-up time on both weekdays and weekends were the latest in the evening type. Sleep duration on weekdays was shorter in the evening type (5.2 h) than in the morning type (6.2 h) and in the intermediate type (5.8

h). The Athene Insomnia
Scale score was the highest in the evening type, however there was no difference in daytime sleepiness (Epworth Sleepiness Scale score) among chronotype groups. Among those identi ed as evening type, no students had a symptom of early morning awakening, while 19% of students had these symptoms in the morning type. The prevalence of di culty awakening was higher in the evening type (70%) than in the morning type (15%). Chronotype and eating pattern Eating patterns in each chronotype were shown in Table 4. Breakfast and dinner time were the earliest in morning type. At breakfast, evening type had the shortest meal time. At every meal, the percentages of skipping meals were the highest (65% for breakfast, 21% for lunch and 27% for dinner) in the evening type than in other chronotypes. Although there was no difference in body mass index among choronotype groups, the percentage of the students who gained body weight after entering university was higher in the evening type (45%) than in the intermediate type (29%) and in the morning type (35%).  The percentages of the nursing students who have experienced absence, tardiness, falling asleep during class and/or interference with academic achievement were higher in the evening type than in other chronotypes (Table 5).

Chronotype and lifestyle/social activities in nursing students
The present study revealed that as high as 18% of Japanese female nursing students were identi ed as evening type. Furthermore, living alone, engaging in a part-time job and/or club activity were associated with evening type after adjusting for confounding factors. The students who live alone can make their life schedule themselves, independent of their family, which promotes delay of circadian rhythm. On the contrary, engagement in a club activity may restrict and properly regulate students' life schedule.
Although detailed information regarding club activities could not be obtained in the present study, further investigation of this issue is warranted. Among the students with evening type, as high as 89% of them had a part-time job. In addition, 38% of them were engaged in a part-time job after 10 p.m. The adjusted odds ratio of having a part-time job on evening type was 3.5 (95% con dence interval: 1.3-9.3), con rming that a part-time job can be a risk factor for having a later chronotype. Thus, durationand frequency of time spent engaged in a part-time job should be considered to keep students on a proper sleep-wake schedule.
The present study also revealed an association between skipping meals and chronotype. Many previous studies have reported an association between skipping breakfast and evening type (27,44,45). Skipping breakfast is unhealthy eating behavior which contributes to metabolic disorders including obesity and diabetes (46,47). In the present study, skipping lunch and dinner was associated with chronotype as well as skipping breakfast. This may suggest that their dietary schedule regulated by circadian rhythm is collapsed as well as their sleep-wake schedule. The percentage of the students who gained weight after entering university was higher in the evening type although there was no difference in body mass index among chronotypes. According to previous studies, chronotype is associated with food preference/intake; evening type individuals had a higher intake of energy, sucrose, fat and saturated fatty acids than morning type individuals(28). In contrast, morning type individuals had a higher intake of fruit(48).
Although information regarding food intake could not be obtained in the present study, a preference for unhealthy food intake may cause weight gain after students with evening type enroll in university.
Nursing students study the importance of nutrition, sleep and physical activity for health, and its mechanism as part of nursing. They are required to understand that circadian rhythm at their age is biologically prone to delay and that a regular life-schedule is important to adequately maintain their physical/mental health and academic performance. For nursing students and nursing teachers, knowledge of sleep disorders including insomnia, circadian rhythm disorder, and hypersomnia needs to be disseminated. In the present study, one-third of the students with evening type had di culty initiating sleep even though their sleep duration was insu cient (5.2 h on weekdays). This is because they suffer from insomnia and/or their endogenously delayed circadian rhythm disturbs the process of falling asleep. A medical approach is needed in the case that a sleep problem cannot be solved by a student's own effort.
Chronotype and health-related quality of life / academic performance Chronotype was associated with mental health-related quality of life but not with physical health-related quality of life. In mental health-related quality of life, the score was lower in the evening type and intermediate type than in the morning type. In middle-aged or older adults, late chronotype was associated with poor physical health-related quality of life (4). However, in the young population the impact of late chronotype on physical health-related quality of life was not apparent. It can be considered that long-term late sleep-wake rhythm and following insu cient sleep bring about future lifestyle-related disease occurring after middle age.
Regarding academic performance, more than half of the evening type nursing students experienced absences and tardiness, and almost all the students had experience falling asleep during class. Nursing students face busy schedules due to a challenging curriculum consisting of practical training, study for registered nurse licensure exams, and completion of a graduation thesis. Thus, maintaining healthy lifestyle is important for them.

Limitations
The present study had some limitations. First, the survey was conducted during the course of normal classes. According to some previous studies, nursing students experience stress during practical training (49,50). During practical training, their sleep patterns and the effect of chronotype on healthrelated quality of life / academic performance may differ from the results of this study. Secondly, the causal relationship between chronotype and outcomes could not be ascertained in this cross-sectional study. Finally, we analyzed data from only female nursing students. Eveningness is more severe in men than in women(1); therefore, the impact of chronotype on health-related quality of life / school performance in male nursing students may differ from that of female students. Further longitudinal studies including a sleep survey during practical training in both male and female nursing students are needed in the future.

Conclusions
The present study revealed chronotypes among Japanese female nursing students. Late chronotype was associated with living alone, having a part-time job, engaging in club activities, and an unhealthy lifestyle, including delayed sleep-wake phase, insu cient sleep, and skipping of meals. The students with evening type and intermediate type had poor mental health-related quality of life than those with morning type. Most of the evening type nursing students experienced absences, tardiness and falling asleep during class. Education of sleep hygiene and a healthy lifestyle to prevent late sleep-wake rhythm would contribute to improve nursing students' health-related quality of life / academic performance.

Declarations
Ethics approval and consent to participate Ethical approval for this survey was granted by the Ethical Committee of the Institute of Neuropsychiatry (No.162). All the subjects participated on a voluntary basis and responses were treated anonymously.
Written informed consent was obtained from the participants.

Consent for publication
Not applicable Availability of data and materials