The Association between Sleep Duration, Breakfast Routine and Nutritional Status in Indonesian Adolescents during COVID-19 Pandemic

Background : Adolescents are susceptible to nutritional status issues, both undernutrition, and over-nutrition, becoming a public health concern promptly. There were 912 junior and high-school adolescents who were obese and 249 high-school adolescents who had low body mass index (BMI) in Samarinda City. During the COVID-19 pandemic, adolescents experienced changes in sleep duration, and many adolescents were skipping breakfast. Sleep duration and breakfast can affect the nutritional condition of adolescents. Objectives : The purpose of this study was to determine the association between sleep duration, breakfast routine and BMI in Samarinda, Indonesian adolescents during COVID-19 pandemic. Materials and Methods : A total of 340 adolescents was sampled and assessed using a cross-sectional technique to ascertain their sleep duration, breakfast routine, and nutritional status. Nutritional status was classified based on BMI-for-age and z-value BMI. The amount of sleep duration was calculated by the average wake time and sleep time. Breakfast routine was obtained from seven days of breakfast before 9 am. Then, using multivariate analyses were tested for sleep duration, BMI z-value, breakfast routine, and nutritional status. Results : This study revealed that 68.5% had good nutrition, with an average sleep duration of 8 hours (65.9%) and irregular breakfast (59.1%). Nutritional status was significantly influenced by breakfast routine (p=0.044), gender (p<0.001), and mother’s employment (p<0.001). A cubic association was found between sleep duration and BMI (p=0.045); and a significant association between breakfast routines and BMI, independent from age, gender, ethnicity, school. Conclusion : Adolescents must consider their sleep duration and the frequency and composition of their breakfast. Future study in the longitudinal study is needed to explore in more detail.

relationship between sleep duration and the z value of BMI, which was seen from the significant fixed effects results. Linear, quadratic, and cubic tests were adapted to the four models. For all tests, a two-tailed p-value < 0.05 was considered statistically significant.
The group with the highest number of good nutritional status was 16 years. In addition, the number of poor nutrition (undernutrition, overnutrition, and obesity) was only 43 respondents. There are 28 respondents aged 17 years who have more nutritional status and obesity, which makes this age has the highest number compared to other ages. The good nutritional status was predominantly female, while the malnutrition was predominantly male. In addition, respondents whose father is a goverment/private employee have the best nutritional status, amounting to 105 respondents. At the same time, they also have the highest number of over nutritional status compared to other fathers' occupations, which are 23. Based on the mother's occupation, respondents with a housewife mother have the best nutritional status compared to working mothers.
Based on table 1, the most respondents slept for <8 hours, which amounted to 224 (65.8%). The results of the cross-tabulation showed as many as 158 adolescents had good nutritional status and sleep duration < 8 hours. In addition, respondents with sleep duration < 8 hours had the highest good nutritional status compared to other sleep durations. And, most respondents (59.1%) did not have breakfast regularly. In addition, as many as 131 respondents who do not routinely have breakfast have good nutritional status, while only 26 respondents have poor nutritional status and do not routinely eat breakfast.  Results of the chi-square test showed that gender (<0,001) and mother's occupation (<0,001) were significant. Meanwhile, other variables were not significant. For the cubic test results displayed in table 2, the significance values obtained in model 1, model 2, and model 4 were 0.045, 0.042, and 0.020, which showed significant results with the Z score BMI. However, for model 3, the results were insignificant with the Z BMI value because the significance value obtained was 0.052. The logistic regression statistical test results in table 3 showed the significance value (p-value) in each model of 0.044, 0.061, 0.047, and 0.024. Because p < 0.05, this means that model 1, model 3, and model 4 showed a significant value, while model 2 did not show a significant value.
The results of the cubic test were presented in the figure 1 where it can be seen that the line begins to rise at a sleep duration of fewer than 8 hours, then falls back to 8 to 9 hours of sleep duration and again experiences a high increase when sleep duration was 10 hours. These results showed an increase in the Z score BMI when sleep duration was less than 8 hours and a significant increase was more than 10 hours.

DISCUSSION
This study's main results indicate a relationship between sleep duration and breakfast routine on the nutritional status of adolescents during the COVID-19 pandemic. However, the relationship found between sleep duration and BMI Z value based on the Multicentre Growth Reference Study (MGRS) for sleep duration [31]. In addition, there is also a relationship between gender and mother's occupation with the nutritional status of adolescents.
In term of age, Salmela-Aro (2011) categorized adolescents into three, namely, early adolescents (11-13 years), middle adolescents (14-17 years), and late adolescents (17-19 years) [32]. Therefore, based on the results of this study, 90% of adolescents were included in the category of middle adolescents, and 10% were late adolescents. Drastic growth and development occur at that age, so the need for energy, vitamins, protein, and minerals increase significantly [20] In the current study, the prevalence of overweight and obesity was 22.6% in adolescents aged 17-19 years. These results are very high compared to the results of previous studies, which found the prevalence of overweight and obesity in adolescents is 2.3% [33]. In the same age group, the prevalence of malnutrition was 13.2%, while the study by Roba et al. (2016) reports that 29.5% of adolescents have poor nutritional status [34]. These different results may be caused by different socio-economic backgrounds or ethnic differences in dietary behaviour [34,35]. Strict diet patterns and over snack consumption can also make their nutritional intake unfulfilled and result in malnutrition [36]. While the reason why adolescents with overweight or obesity caused too much consuming fat and carbohydrate food and lack in physical activity [36].
Nutritional issues in adolescents might started during infant period and they also suffer from malnutrition during infant periods. Furthermore, the adolescent environment influences their nutritional status [37]. Nutritional issues in adolescents, such as undernutrition or obesity, can also be induced by an imbalanced adolescent nutritional intake [38]. Food consumption and weight gain in the 10 -19 years age group are rising during the COVID-19 pandemic, potentially affecting their nutritional condition [39]. One can assume that this might be caused by a shift in behavior related to weight increase in the school-age group during the ongoing pandemic [40].
The respondents in this study were predominantly female, with the sex ratio between female and male being 2:1. Adolescents experience different sexual maturity between girls and boys, influencing their nutritional needs [20]. Adolescent sexual maturity is related to hormonal changes, body composition, weight, and linear growth [20]. Gender determines a person's nutritional needs, where male adolescents have higher nutritional needs due to their higher physical activity than female adolescents [41]. Nutritional status in adolescents was found to have a association with gender on this study. This finding is in line with the results of a study conducted by Darling et al. (2020), which found a relationship between adolescent girls with a reduced risk of being underweight, but a high risk of being overweight [42]. Meanwhile, adolescent boys are associated with low body weight [42]. The difference between girls and boys is because girls have about twice as much fat as boys. After all, girls are prone to fat accumulation [43]. Research conducted by Maltoni et al. (2021) stated weight gain in adolescent boys during the COVID-19 pandemic [44].
Women from young to old, married or unmarried, have children or do not have children at this time have the ambition to work, so it is not uncommon to find a mother who has a dual role in a family [45]. However, during the COVID-19 pandemic, many mothers between the ages of 25 and 44 lost their jobs due to demands to care for their families [46]. This study found a relationship between a mother's work and adolescent nutritional status. However, the results of this study were different from previous studies, which reported no relationship between the mother's work and the nutritional status of students [47]. Adolescents with mothers who have employment status as homemakers are the most likely to have good adolescent nutritional status based on this study. Because homemakers have time to meet their children more often, mothers can pay more attention to their children's health [47].
This study found no significant association between father's occupation and adolescent nutritional status. This may be due to the status of mothers who are mostly housewives and the finding of a relationship between mother's occupation status and adolescent nutritional status, so that father's occupation does not show significant results. Meanwhile, a previous study states a significant relationship between fathers' work and adolescent nutritional status [48]. The type of father's occupation affects his income in which will affect the amount and food selection at home [48]. Income that only comes from one parent can hinder overweight in adolescents [49]. Family with low income might have some difficulties to provide and choose nutritious and diverse foods [50].
Sleep duration usually refers to the total amount of sleep gained, either during episodes of nocturnal sleep or over 24 hours [51]. Sleep is defined as a behavioral state characterized by rest, reduced environmental awareness, and immobility [52]. Different sleep times result from different lifestyles and jobs for each individual [52]. When sleep is of insufficient duration, it can disturb consciousness during the day and cause excessive experience sleepiness [52]. Adolescents often experience insufficient sleep duration can be caused by the adolescents deliberately reducing the duration of their sleep for other activities, such as attending parties, working, studying at night for exams [53]. Lack of sleep duration can cause individuals to experience hallucinations, mood swings, fatigue, irritability, impaired perception & orientation, and declining attention [52].
Based on this study, most adolescents had a total sleep duration of less than 8 hours, so this finding was in line with the results of the study by Sinha et al. (2020), which reported that the amount of sleep duration for adolescents during the COVID-19 pandemic is only 4-6 hours in a day [54]. It can be caused by adolescents who deliberately reduce their sleep duration, such as doing activities at night, studying, partying, or working [53]. These results did not meet the sleep needs of adolescents recommended by the Indonesian Ministry of Health in 2018, which is 8-9 hours of sleep duration in one day.
Previous research on sleep duration during the COVID-19 pandemic conducted in five cities (Seoul, Stockholm, London, Los Angeles, and New York) found that the average sleep duration of respondents is less than 8 hours [55]. This short sleep duration is due to increased stress during the COVID-19 pandemic [56]. During the COVID-19 pandemic, many adolescents experienced stress, making it hard for them to sleep at night. Stress and sleep quantity can also reduce sleep duration because during the COVID-19 pandemic, they rarely sleep at night, even though their sleep duration is only about 6 to 8 hours [57].
In addition, poor health can cause adolescents to sleep less than eight hours. Evidence by Panel et al. (2015) states that adolescent sleep duration of fewer than seven hours tends to have poor and low health and low physical and mental quality [58]. Likewise, Guo et al. (2021) state that an unhealthy lifestyle occurred during the COVID-19 pandemic among students at a high level of education [59]. Health problems such as obesity in adolescents, hypertension, diabetes, and cardiovascular disease can cause sleep duration shorter than eight hours [60]. Individuals who lack sleep can affect their long and medium-term performance (58). Short sleep duration can affect changes in sleep quality during the COVID-19 pandemic [61].
Research on sleep duration in America states that, on average, an adolescent sleep for 7.3 hours in one day [62]. This result is similar to the studies conducted in European and North American states, where the average adolescent sleep duration ranges from 7 to 9 hours on school days [63]. In addition, these results are also supported by research conducted in Africa, Asia, Central and South America, the Middle East, the Caribbean, and Oceania, which found that the sleep duration in 16-year-old adolescents is 7 hours [64].
This study found that 15.6% of adolescents had a sleep duration of more than 9 hours, while research conducted by AL-Haifi (2016) found that 24.85% of adolescents have more than 9 hours sleep duration, others found that almost 90% of adolescents have more than 7 hours sleep duration in one day [65,66]. Adolescents with longer sleep duration can increase the risk of coronary heart disease and affect their mental health [67,68].
This study showed that only 18.5% of adolescents met the adequacy of sleep duration, namely for 8-9 hours, while the majority (81.5%) did not meet the adequacy of sleep duration. As a comparison, previous research showed that 82.7% of adolescents met the adequacy of their sleep duration, while 17.2% did not meet the adequacy of their sleep duration [69]. Because other study were conducted before the COVID-19 pandemic while this study was conducted during the pandemic, so that makes results are different. Another reason is adolescents having a tough time maintaining and initiating sleep [70].
The bivariate analysis results showed no significant relationship between sleep duration and adolescent nutritional status during the COVID-19 pandemic. It is in line with the results of a previous study, which stated that there was no association between BMI and sleep duration in adolescence [71]. A study by Schneider et al. (2020) also found that there is no association between BMI and sleep duration in adolescent boys [72]. These results show that short sleep duration does not affect their nutritional status [73].
Sleep duration and nutritional status are not related because when adolescents stay up late, they do not always consume food or drink; it could also be that they are busy doing school assignments [73]. In addition, factors that directly affect nutritional status are food intake and infection, while sleep duration is an indirect factor affecting nutritional status [74]. The absence of this relationship can also be explained that sleep duration is not an independent factor. It can also be caused by other factors such as genetic factors and environmental factors [75].
The results of the cubic test analysis in this study found that adolescents whose sleep duration was more than 9 hours experienced a high increase in their BMI Z value, which was inversely proportional to the findings of Grandner et al. (2015) [76]. They found that a short sleep duration of less or equal to four hours is associated with high BMI Z values. This difference is because a non-linear relationship was found in the current study, while Grandner et al. (2015) found a linear relationship [76]. Lack of sleep duration is associated with unhealthy eating habits, such as more significant portions, increased hunger, increased appetite in high-calorie foods, and increased intake of sugary foods and drinks [77]. Children who experience sleep deprivation and lack healthy food have a high BMI z value [77].
Research from Italy states that adolescents with low or average weight tend to have longer sleep durations compared to adolescents who are overweight and obese [78]. The results of this study are in line with the results of this study, in which 70% of adolescents with low or normal nutritional status had a total sleep duration of more than nine hours compared to adolescents with overweight and obese status. Covariates effect such as lifestyle, diet, and physical activity on BMI can influence these outcomes, as can sample size, age group differences, and geographic and ethnic variations [79].
For breakfast, can be characterised as the first meal before or starting the activity two hours after waking up, usually, less than 10 am, with a calorie content of about 20% to 35% of the total daily energy adequacy [19]. This study found that 59.1% of adolescents did not regularly eat breakfast. These results align with Hermanto et al.'s (2020) research, which found that 70.4% of adolescents rarely eat breakfast [70]. Skipping breakfast is often done by adolescents and can reduce their nutrient intake [20].
Adolescents skip breakfast because there is no food available in their homes [22]. Husain & Ashkanani (2020) reported that during the COVID-19 pandemic, breakfast is often missed. Staying up late makes someone snack in the middle of the night, and excessive sleep is the reason for skipping breakfast [80]. Other reasons adolescents skip breakfast are lack of appetite, no time, difficult to make a food, and religious reasons [81]. These results are inversely proportional to the research conducted by Sidor & Rzymski (2020), who stated that 65.5% of respondents had breakfast every day [82].
A total of 131 adolescents who did not regularly take breakfast has good nutritional status, while adolescents who regularly eat breakfast with good nutritional status are 102 respondents. Based on this study, adolescents who did not regularly eat breakfast tend to have good nutritional status during the COVID-19 pandemic. It can be due to other factors related to good nutritional status, such as physical activity. Adolescents who are physically active during the COVID-19 pandemic tend to have normal nutritional status [83]. In addition, the intake of energy, carbohydrates, and protein also affects the nutritional status of adolescents [84]. Therefore, there is a possibility that adolescents have good nutritional status but do not regularly eat breakfast.
The bivariate analysis results in this study showed no correlation between breakfast routine and nutritional status. A previous study by Kurniawan (2020) show no relationship between breakfast routines and nutritional status [85]. A typical breakfast cannot determine a person's nutritional status because the total energy requirement obtained from breakfast food is only 25% [38]. So, a balance breakfast menu is needed to fulfill the daily nutritional intake [86]. Previous studies demonstrated that there is no association between breakfast habits and the nutritional status in high school students [85,87]. Food quality and quantity such as large portions, nutritional value, and food varieties affect a person's nutritional status rather than solely breakfast behavior [88].
This study found a linear relationship between breakfast routine and nutritional status in adolescents. Nutritional status is a balance between nutrient intake from food and the nutritional needs needed for body metabolism [2]. Data analysis using logistic regression tests found an association between breakfast routines and nutritional status in adolescents. This finding aligns with Amalia & Adriani (2019), which found an association between breakfast routines and nutritional status [89]. Research conducted on European and Brazilian adolescents found that skipping breakfast leads to obesity in adolescents [90]. Similarly, a study in Bangladesh and India demonstrated that skipping breakfast significantly correlates with being overweight [91]. However, research from Zagreb, Croatia, states that adolescent girls who eat breakfast have a higher incidence of obesity [92].
Adolescents who skip breakfast tend to have increased blood sugar levels, fatigue, declined concentration, and experience a decrease in physical and mental conditions [93]. Breakfast can improve cognitive performance, as the adolescents will not be disturbed by hunger and affect memory [94]. A previous study have reported that skipping breakfast is associated with an increased risk of obesity by 1.75 times than eating breakfast regularly [19].
During the COVID-19 pandemic, adolescents increase their breakfast and unhealthy food/drinks consumption, resulting in weight gain that affects their nutritional status [95]. Beside excessive breakfast, skipping breakfast can also increase the energy intake obtained when adolescents consume snacks to replace breakfast [96]. Another explanation is that adolescents who skip breakfast during the COVID-19 pandemic are caused by waking up at night, leading to snacking in the middle of the night and also excessive sleep the next day, which can lead to overweight and obesity [80]. Another study conducted in South Korea stated that in general breakfast consumption in adolescent during the pandemic COVID-19 is higher than before the pandemic. During the pandemic period, adolescents have a lot of free time to eat at home, the ban on going out causes adolescents to have a lot of time to eating or snacking at home [97]. Also, a study showed that during a pandemic there are some people who skip breakfast, which can affect their quality of life [98].

CONCLUSION
In a nutshell, there was an association between sleep duration and breakfast routine with adolescent nutritional status. The findings indicated that many adolescents had less than 8 hours of sleep duration and a lack of breakfast routines. However, more than half of adolescents had good nutritional status. Adolescents are advised to get enough sleep duration as recommended and to have breakfast every day and maintain it during the COVID-19 pandemic.