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Circadian pattern of sleep, energy expenditure, and body temperature of young healthy men during the intermittent fasting of Ramadan
Appetite 54 (2010) 426–429
Contents lists available at ScienceDirect
Appetite journal homepage: www.elsevier.com/locate/appet
Short communication
Circadian pattern of sleep, energy expenditure, and body temperature of young healthy men during the intermittent fasting of Ramadan Ahmed BaHammam *, Mohammad Alrajeh, Mohammad Albabtain, Salman Bahammam, Munir Sharif The University Sleep Disorders Center, College of Medicine, King Saud University, Riyadh, Saudi Arabia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 September 2009 Received in revised form 18 January 2010 Accepted 19 January 2010
We hypothesize that factors other than a sudden shift in eating habits contribute to delay of circadian rhythms during Ramadan. We assessed circadian changes during a baseline period (BL, 1 week before Ramadan), the first week (R1), and the second week (R2), of Ramadan, in six healthy Muslim young adults using portable armband physiological and activity sensor devices. All participants lived in an unconstrained environment and showed delayed sleep phase syndrome, so that they normally slept during the day and ate at night. During Ramadan, there was a further delay in the acrophase of skin temperature during Ramadan, indicating a shift in the circadian pattern of body temperature. Additionally, there was a delay in the peak of energy expenditure during R1 and R2. These results support our hypothesis that in addition to sudden shift in meal times, other factors may affect the sleep pattern and circadian rhythms during Ramadan. ß 2010 Elsevier Ltd. All rights reserved.
Keywords: Ramadan Fasting Circadian pattern Energy expenditure Temperature Sleep
Introduction Investigators have long recognized that experimental fasting modifies the sleep patterns of various species, in that fasting increases wakefulness and markedly reduces rapid eye movement (REM) sleep (Borbely, 1977; Danguir & Nicolaidis, 1979; Rashotte, Pastukhov, Poliakov, & Henderson, 1998). However, the results of experimental fasting cannot be extrapolated to Ramadan fasting for several reasons. First, Ramadan fasting is intermediate, in that there is abstinence from food, drink, and smoking only between dawn and sunset. Eating is allowed after sunset, and thus results in a sudden delay in the timings of meals which may theoretically impact of the circadian pattern of body temperature and sleep (BaHammam, 2004; Roky et al., 2003). Second, Ramadan follows the lunar calendar and occurs 11 days earlier every year and thus gradually changes seasons over several years. The duration of fasting from dawn to dusk is longer in the summer than in the winter, particularly for followers who live far from the equator. Third, there are changes in day–night activity patterns, such as rising for the pre-dawn meal (Suhur) and prayer. Finally, the long duration of Ramadan fasting (1 month) may allow physiological adaptations. Therefore, the physiological and behavioral changes occurring during Ramadan fasting may differ from those observed in experimental fasting (Azizi, 2002).
* Corresponding author at: Sleep Disorders Center, College of Medicine, Department of Medicine 38, King Saud University, Box 225503, Riyadh 11324, Saudi Arabia. E-mail addresses: [email protected], [email protected], [email protected] (A. BaHammam). 0195-6663/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.appet.2010.01.011
Few studies have examined sleep patterns during Ramadan fasting. Most such studies used questionnaires to assess the sleep patterns of individuals who were working or studying during the daytime (fasting). Two reports investigated sleep architecture objectively by use of an overnight sleep study, but the results were contradictory regarding total sleep time (BaHammam, 2004; Roky et al., 2003). Some of the changes associated with Ramadan fasting may impact sleep patterns, circadian rhythms, and the biological clock during that month. The eating of meals exclusively at night has been proposed to modify circadian rhythms (Roky, Chapotot, Hakkou, Benchekroun, & Buguet, 2001). Body temperature normally follows such a rhythm, rising during the day and falling at night (BaHammam, 2003). Exclusive eating at night may cause increases in body temperature at night and thereby delay the circadian patterns of body temperature and sleep (Roky et al., 2001). Nevertheless, conflicting data have been reported regarding the effects of Ramadan fasting on the circadian pattern of sleep and other physiological parameters. Lifestyle changes like delay in starting schools and work, increased activity in malls until late at night, broadcasting popular programs in TV channels until dawn, conducting prayers at night and sometimes until 2–3 AM, social gathering with families and friends until late at night have been suggested as potential causes of delay in circadian rhythms during Ramadan (BaHammam, 2005, 2006). In particular, many social and family activities occur at night during Ramadan and this may encourage participants to delay bedtimes. We hypothesize that lifestyle changes other than night-time eating may contribute to the delay in the circadian rhythm seen during Ramadan. This study assessed objective circadian changes
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in sleep, energy expenditure, and body temperature during Ramadan fasting in a free-living environment. We studied healthy young adults who had delayed sleep phase syndrome (DSPS) and were on vacation during the study period. Our group of volunteers during the non-Ramadan period typically slept during daytime and were wake and eating at night, so we expected that the impact of Ramadan fasting on their eating habits would be less than that for subjects with normal sleep pattern. Nevertheless, other lifestyle changes during Ramadan may influence circadian rhythms. Materials and methods Study group This study was conducted during the last week of Shaaban (the eighth month of the Islamic year, baseline, BL), and the first (R1) and second (R2) weeks of Ramadan (the ninth month of the Islamic year) 1429 Hijra (corresponding to August 23, 2008 to September 14, 2008). The study group consisted of a non-random sample of seven young healthy Muslim male non-smoking University students, age 18–24 years, whose DSPS chronotypes were ‘‘evening-type’’, based on an abridged version of the Horne and ¨ stberg questionnaire (a questionnaire that establishes three O behavioral categories: morning type, neither type, and evening type) (Adan & Almirall, 1991). Sleep patterns were monitored for 2 weeks prior to the commencement of the study by use of sleep diaries. We observed no shift or change in bedtime or wake-up time during this initial monitoring period. The student participants were on their summer break, so did not have any classes. No participant was employed during the study period. All volunteers were interviewed and assessed by a sleep specialist to ensure that they did not have sleep complaints. Information about the time and frequency of meals was collected on daily basis. We defined major meals as daily meals that included more that one food and a beverage and the participants had the option to name more than one meal as a major meal (Oltersdorf, Schlettwein-gsell, & Winkler, 1999). Informed consent was obtained from all participants and the protocol was approved by the Ethics Committee of our institute. One of the participants was subsequently excluded as his armband did not collect data during the baseline period. Study protocol Before starting the study, participants reported to the Sleep Disorders Center (SDC) where age, height, weight, and vital signs were recorded and each subject was given training and orientation. According to the manufacturer’s instructions, each participant was asked to wear a SenseWear armband on the triceps of his right arm, over the triceps muscle, at the midpoint between the acromion and olecranon processes. The armband was removed only during swimming and showering. Participants reported to the SDC twice during the study period to download data and charge batteries. Armband The SenseWear Pro ArmbandTM (Body Media, Pittsburgh, PA) is a portable sensing device 8.8 cm 5.6 cm 2.1 cm in size and 82 g in weight. The device measures skin temperature, galvanic skin response, heat flux, and body acceleration (movement). Additionally, the device places the above-measured parameters and descriptive characteristics of the participant (gender, age, height, weight) into proprietary algorithms that report total and active energy expenditure, metabolic equivalent (METS), duration and quantification of physical activity, body position, sleep efficiency, and sleep duration. Technical characteristics of the Armband have been described previously (Dorminy, Choi, Akohoue, Chen, & Buchowski, 2008).
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Accelerometry is measured using a two-axis micro-electronic mechanical sensor. Heat flux is assessed employing a proprietary sensor that incorporates thermal-resistant materials and thermocouple arrays. Galvanic skin response is used as an indicator of evaporative heat loss and is measured using two hypoallergenic stainless steel electrodes. Skin temperature is assessed using a thermistor-based sensor. The measured skin temperature is continuously and linearly indicative of core activities in the body (Teller, 2004). Data provided by the manufacturer showed that skin temperature sensor accuracy was at 0.1 8C in the interval 0– 70 8C. The sensor was calibrated at room temperature (23–25 8C) and these data was stored for offset correction on a scale of 0–50 8C and a resolution of 0.018 8C per A/D tick. Proximal skin temperature follows the same circadian rhythm as does rectal temperature (Krauchi & Wirz-Justice, 1994). The near-body temperature sensor measured the temperature of the cover on the side of the armband and provided information on total energy expenditure. Each sensor was monitored 32 times per second, and data tracked over a period of 1 min (Teller, 2004). Minute-by-minute data from the Armbands were analyzed by algorithms using Body Media1 InnerView1 Research Software (version 5.1) provided by BodyMedia, Inc. (Malvolti et al., 2005). The commercial energy expenditure algorithm was validated by use of double-labeled water (Mignault, St Onge, Karelis, Allison, & Rabasa-Lhoret, 2005) and metabolic carts (Jakicic et al., 2004; Malavolti et al., 2007). In addition, the SenseWear Armband has been validated for study of sleep patterns, as the internal body media algorithm can identify sleep and wakefulness with moderate-to-high sensitivity, specificity, and accuracy (Miwa, Sasahara, & Matsui, 2007; Teller, 2004). The American Academy of Sleep Medicine (AASM) has indicated that actigraphy (the use of devices that monitor body movements) can be a useful adjunct in the diagnosis of circadian rhythm disorders (Littner et al., 2005). ‘‘Total Sleep Time’’ (TST) was defined as the main consolidated sleep period and ‘‘Nap’’ as any other brief period of sleep. Statistical analysis Data in the form of MS Excel spreadsheets were downloaded from each ArmbandTM using Body Media1 ‘‘InnerView1 Professional 5.1. Data for each subject was analyzed individually. For heat flux, skin temperature, near-body temperature, energy expenditure, and METS, data were analyzed and averages were calculated as follows: overall weekly average, overall hourly average for each day, and hourly average for each week. We developed a 24 hcosinor model ( f ðtÞ ¼ M þ A Cosðð2pt=TÞ þ ? Þ; where M = Mesor; A = Amplitude; Ø = Acrophase; T = 24 h) to get the best estimates of the overall acrophase for Skin Temperature and Energy Expenditure. The model was executed for each subject’s data during the three periods. Data was expressed as means SD. Comparisons among BL, R1, and R2 were performed using one-way repeated-measures ANOVA for all variables. Results were considered statistically significant if p values were 0.05. When the difference was significant, post hoc testing was performed using pairwise comparison. Effect size was calculated using partial eta-squared test. Effect size was considered large if the value was .14 (Cohen, 1992). All the participants named one meal per day as a major meal, hence, we named that meal ‘‘the main meal’’ in the results. Standard statistical software (SPSS Version 16.0; SPSS Inc. Chicago, IL) was used for all statistical analysis. Results The mean age of participants was 20.5 2.9 years and the mean body mass index (BMI) was 22.6 2.7 kg/m2. There were no significant changes in BMI throughout the study. Table 1 shows data
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Table 1 Comparison between baseline (BL), and first (R1) and second (R2) weeks of Ramadan. Variable
BL
R1
R2
Number of meals per day Time of the main meal (24 h) Bed time (24 h) Wake time (24 h) TST (h) NAP duration (h) TST + NAP (h) Time of NAP (24 h) Heat flux
2.27 0.82 21.60 1.14 4.0 1.4 10.42 1.87 6.42 1.27 1.61 0.77 7.88 1.19 13.42 1.82 63.76 6.88
2.33 0.52 20.00 2.74 5.6 1.3 12.68 1.41Ü 7.08 0.57 2.08 0.88 9.01 0.91 14.41 1.51 63.9 9.4
2.50 0.55 19.50 2.81 5.42 2.6 11.76 2.32 6.34 0.75 1.94 0.53 8.13 1.07 14.12 0.56 63.9 9.4
Skin temperature (8C) Mesor Amplitude *Acrophase (24 h)
33.14 0.34 0.84 0.67 20.43 1.67
33.22 0.33 0.60 0.71 22.24 1.25
33.24 0.2 0.69 0.73 22.93 1.55
Energy expenditure (kcal/min) *Mesor Amplitude *Acrophase (24 h) *METS
2.28 0.36 1.01 0.38 20.34 1.77 1.88 0.22
2.11 0.35Ü 0.92 0.36 22.38 1.37Ü 1.74 0.16Ü
2.13 0.28 0.85 0.30 22.22 1.73Ü 1.75 0.15
BL: baseline; R1: first week of Ramadan; R2: second week of Ramadan; TST: total sleep time; METS: metabolic equivalent. * P < 0.05 based on repeated measured ANOVA (overall group differences). Ü The difference is statistically significant compared to baseline (p < 0.05) when paired wise comparison were made.
collected during BL, R1, and R2. There were no significant differences in the number of meals or the timing of the main meal between BL and Ramadan. During BL, the participants inconsistently took light meals after awakening (11.25 1.3) and between 02:00 and 03:00 AM (2.6 0.9). During Ramadan, all the participants took a light meal at sunset (time of sunset ranged from 05:59 to 06:21 depending on the date of the month) to break their fast, which consists of a few dates and a drink of water or juice and inconsistently took a light meal (Suhur) before Dawn between 02:00 and 03:45 AM (R1: 2.8 0.5 and R2: 2.9 0.4) (dawn occurred between 04:05 and 04:21 depending on the date of the month). The partial eta-squared statistics indicated large size effect for the delay in bedtime during Ramadan (.27). Wakeup time was delayed during Ramadan (R1 and R2) compared to BL. The difference between BL and R1 was statistically significant (10.42 1.87 vs. 12.68 1.41). Whereas TST was comparable during the three periods, TST + nap time was longer during Ramadan than in BL with a large effect size as indicated by partial eta-squared statistics (.33). Energy expenditure and METS were significantly lowered during Ramadan. There was delay in the acrophase of skin temperature during Ramadan, compared to BL. In other words, there was a shift in the circadian pattern of body temperature during Ramadan. Additionally, there was a delay in the acrophase of energy expenditure during Ramadan. Discussion The current study demonstrated that the major sleep period was delayed as evidenced by a marginally significant delay of bedtime (large effect size) and significant delay of wake-up time, during Ramadan. Additionally, temperature acrophase (i.e., the times at which the maximum values occurred in the circadian cycle), and maximum energy expenditure were delayed. Importantly, our study subjects were young men who did not greatly change their eating habits during Ramadan. These results support our hypothesis that factors other than fasting, such as cultural and lifestyle changes, may cause a shift in the circadian pattern. Previous studies have suggested that a delay in the circadian pattern and a change in chronotype during Ramadan (BaHammam, 2005; Roky et al., 2001). However, most previous studies enrolled
subjects who were working during the day or attending classes and made significant changes to eating habits during Ramadan. None of our subjects had daytime commitments and all had an eveningtype chronotype, thus minimizing the effect of changing the timing of meals. Additionally, previous studies did not control for the practice used in some Muslim countries of delaying the starting time of work and schools by 2–3 h during Ramadan (BaHammam, 2006). It is known that delays in wake-up time can delay circadian phase significantly and hence temperature rhythm (Taylor, Wright, & Lack, 2008). Our studied subjects had no daytime commitments during the study period and their bedtime and wake-up times were stable for 2 weeks during the baseline period prior to the beginning of the study. A study assessed the chronotype of fasting and non-fasting individuals during Ramadan in Saudi Arabia using an abridged ¨ stberg questionnaire (morningness/ version of the Horne and O eveningness test) (BaHammam, 2005). Interestingly, a change in chronotype was seen in non-fasting non-Muslim residents during Ramadan, with an increase in neither-types and a decrease in morning-types at the beginning and end of Ramadan suggesting that factors other than changes in meals timing may be involved (BaHammam, 2005). Previous studies have monitored body temperature as a marker of circadian pattern during Ramadan (BaHammam, 2004; Roky et al., 2001; Roky, Iraki, HajKhlifa, Lakhdar Ghazal, & Hakkou, 2000). In general, body temperature falls during sleep and rises at wake time. Roky and associates monitored rectal temperature for 24 h in a sample of fasting individuals during Ramadan (Roky et al., 2001). The cited authors reported a delay in the occurrence of acrophase and a reduction in the amplitude of core body temperature during Ramadan. Another study which measured oral temperature confirmed these results. This latter study showed a significant rise in body temperature at 23:00 and 00:00 h and a significant reduction at 09:00, 11:00, 13:00, and 16:00 h (Roky et al., 2000). However, a third study found no significant change in the circadian pattern of oral temperature at 08:00, 16:00, and 00:00 h during the first and third weeks of Ramadan (BaHammam, 2004). Levels of the hormone melatonin also provide a reliable and reproducible marker of circadian changes in humans (Arendt, 1995). Two studies found that a smaller delayed night peak and a flatter slope of serum concentration of melatonin during Ramadan (BaHammam, 2004; Bogdan, Bouchareb, & Touitou, 2001). To the best of our knowledge, no study has previously examined the circadian pattern of energy expenditure during Ramadan. However, examinations of the circadian pattern of energy expenditure in humans have yielded conflicting results. In one study, Consoli and co-workers examined the effect of different meal times on the circadian pattern of energy expenditure in 15 subjects, by measurement of O2 consumption and CO2 production (Consoli et al., 1981). These authors concluded that meal-time did not affect the circadian rhythm of energy expenditure and suggested that the rhythm is endogenous. In our subjects, there was a delay in the peak of energy expenditure, of about 2 h, during R1 compared to BL. This delay continued during the second week of Ramadan and coincided with our measured changes in skin temperature. In general, exercise is best tolerated when the resting body temperature is highest (Atkinson & Reilly, 1996). Thus, we observed a delay in energy expenditure even though eating time did not change significantly during the study period. The current study demonstrated rapid changes in bedtime and wake-up time during Ramadan, in agreement with previous work (BaHammam, 2003, 2005; Roky et al., 2001). Such obvious changes reported in previous studies may be partially explained by delays in starting work during Ramadan (BaHammam, 2006). Nevertheless, a delay in bedtime during Ramadan also occurred in nonfasting residents of Saudi Arabia whose work commencement time
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did not change (BaHammam, 2005). This supports our hypothesis that lifestyle changes other than fasting may cause a shift in circadian pattern during Ramadan (BaHammam, 2005). Data on sleep duration during Ramadan varies with country and these differences seem to be related to lifestyle and cultural differences (BaHammam, 2006). In a sample of university students in Morocco, night-time sleep duration decreased significantly during Ramadan (Taoudi Benchekroun, Roky, Toufiq, Benaji, & Hakkou, 1999). Another study in the United Arab Emirates reported a decrease in night-time sleep duration in university students, but this was compensated by daytime naps (Margolis & Reed, 2004). On the other hand, studies in Saudi Arabia reported no difference in night-time sleep duration or total sleep time (nighttime + naps) during Ramadan (BaHammam, 2003, 2005). The present study, which enrolled Saudi students, is in agreement with the above two studies concerning the role of lifestyle and cultural differences on changes in circadian patterns during Ramadan. The current study has some limitations that need to be addressed. First, the number of recruited volunteers is relatively low. Nevertheless, this limitation is inherent to studies like this that use objective assessment within a short specified period (BaHammam, 2004; Roky et al., 2003; Roky et al., 2001). A larger sample would be necessary to identify predictors of circadian rhythm delay during Ramadan. Second, despite the fact that we recruited volunteers with DSPS to ameliorate the sudden shift in the circadian pattern of caloric intake, the time of meals during BL did not coincide precisely with the time of meals during R1 and R2. However, the timing of the main meal was not significantly different during the three periods and the results did demonstrate a shift in the acrophase of temperature. In summary, we used a validated portable device to measure sleep pattern, skin temperature, and energy expenditure in a small group of young healthy men with evening chronotypes who did not significantly change their eating habits during Ramadan. With the onset of Ramadan, we observed clear delays in bedtime and wake-up time, and in the circadian rhythms of skin temperature and energy expenditure. These findings support our hypothesis that factors other than fasting and mealtime can affect sleep patterns and circadian rhythms during Ramadan. We suggest that future studies seek to identify these factors and monitor the same physiological parameters in fasting and non-fasting individuals during Ramadan. Acknowledgements This project was supported by a grant from the University Sleep Disorders Center of King Saud University and King Abdulaziz City for Science and Technology. The authors would like to thank Dr. Shaffi Shaikh from the Department of Family Medicine, King Saud University for the statistical review. References ¨ stberg morningness–eveningness questionAdan, A., & Almirall, H. (1991). Horne & O naire: a reduced scale. Personality and Individual Differences, 12, 241–253. Arendt, J. (1995). Melatonin and the Mammalian Pineal Gland. London, UK: Chapman & Hall.
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Contents lists available at ScienceDirect
Appetite journal homepage: www.elsevier.com/locate/appet
Short communication
Circadian pattern of sleep, energy expenditure, and body temperature of young healthy men during the intermittent fasting of Ramadan Ahmed BaHammam *, Mohammad Alrajeh, Mohammad Albabtain, Salman Bahammam, Munir Sharif The University Sleep Disorders Center, College of Medicine, King Saud University, Riyadh, Saudi Arabia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 September 2009 Received in revised form 18 January 2010 Accepted 19 January 2010
We hypothesize that factors other than a sudden shift in eating habits contribute to delay of circadian rhythms during Ramadan. We assessed circadian changes during a baseline period (BL, 1 week before Ramadan), the first week (R1), and the second week (R2), of Ramadan, in six healthy Muslim young adults using portable armband physiological and activity sensor devices. All participants lived in an unconstrained environment and showed delayed sleep phase syndrome, so that they normally slept during the day and ate at night. During Ramadan, there was a further delay in the acrophase of skin temperature during Ramadan, indicating a shift in the circadian pattern of body temperature. Additionally, there was a delay in the peak of energy expenditure during R1 and R2. These results support our hypothesis that in addition to sudden shift in meal times, other factors may affect the sleep pattern and circadian rhythms during Ramadan. ß 2010 Elsevier Ltd. All rights reserved.
Keywords: Ramadan Fasting Circadian pattern Energy expenditure Temperature Sleep
Introduction Investigators have long recognized that experimental fasting modifies the sleep patterns of various species, in that fasting increases wakefulness and markedly reduces rapid eye movement (REM) sleep (Borbely, 1977; Danguir & Nicolaidis, 1979; Rashotte, Pastukhov, Poliakov, & Henderson, 1998). However, the results of experimental fasting cannot be extrapolated to Ramadan fasting for several reasons. First, Ramadan fasting is intermediate, in that there is abstinence from food, drink, and smoking only between dawn and sunset. Eating is allowed after sunset, and thus results in a sudden delay in the timings of meals which may theoretically impact of the circadian pattern of body temperature and sleep (BaHammam, 2004; Roky et al., 2003). Second, Ramadan follows the lunar calendar and occurs 11 days earlier every year and thus gradually changes seasons over several years. The duration of fasting from dawn to dusk is longer in the summer than in the winter, particularly for followers who live far from the equator. Third, there are changes in day–night activity patterns, such as rising for the pre-dawn meal (Suhur) and prayer. Finally, the long duration of Ramadan fasting (1 month) may allow physiological adaptations. Therefore, the physiological and behavioral changes occurring during Ramadan fasting may differ from those observed in experimental fasting (Azizi, 2002).
* Corresponding author at: Sleep Disorders Center, College of Medicine, Department of Medicine 38, King Saud University, Box 225503, Riyadh 11324, Saudi Arabia. E-mail addresses: [email protected], [email protected], [email protected] (A. BaHammam). 0195-6663/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.appet.2010.01.011
Few studies have examined sleep patterns during Ramadan fasting. Most such studies used questionnaires to assess the sleep patterns of individuals who were working or studying during the daytime (fasting). Two reports investigated sleep architecture objectively by use of an overnight sleep study, but the results were contradictory regarding total sleep time (BaHammam, 2004; Roky et al., 2003). Some of the changes associated with Ramadan fasting may impact sleep patterns, circadian rhythms, and the biological clock during that month. The eating of meals exclusively at night has been proposed to modify circadian rhythms (Roky, Chapotot, Hakkou, Benchekroun, & Buguet, 2001). Body temperature normally follows such a rhythm, rising during the day and falling at night (BaHammam, 2003). Exclusive eating at night may cause increases in body temperature at night and thereby delay the circadian patterns of body temperature and sleep (Roky et al., 2001). Nevertheless, conflicting data have been reported regarding the effects of Ramadan fasting on the circadian pattern of sleep and other physiological parameters. Lifestyle changes like delay in starting schools and work, increased activity in malls until late at night, broadcasting popular programs in TV channels until dawn, conducting prayers at night and sometimes until 2–3 AM, social gathering with families and friends until late at night have been suggested as potential causes of delay in circadian rhythms during Ramadan (BaHammam, 2005, 2006). In particular, many social and family activities occur at night during Ramadan and this may encourage participants to delay bedtimes. We hypothesize that lifestyle changes other than night-time eating may contribute to the delay in the circadian rhythm seen during Ramadan. This study assessed objective circadian changes
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in sleep, energy expenditure, and body temperature during Ramadan fasting in a free-living environment. We studied healthy young adults who had delayed sleep phase syndrome (DSPS) and were on vacation during the study period. Our group of volunteers during the non-Ramadan period typically slept during daytime and were wake and eating at night, so we expected that the impact of Ramadan fasting on their eating habits would be less than that for subjects with normal sleep pattern. Nevertheless, other lifestyle changes during Ramadan may influence circadian rhythms. Materials and methods Study group This study was conducted during the last week of Shaaban (the eighth month of the Islamic year, baseline, BL), and the first (R1) and second (R2) weeks of Ramadan (the ninth month of the Islamic year) 1429 Hijra (corresponding to August 23, 2008 to September 14, 2008). The study group consisted of a non-random sample of seven young healthy Muslim male non-smoking University students, age 18–24 years, whose DSPS chronotypes were ‘‘evening-type’’, based on an abridged version of the Horne and ¨ stberg questionnaire (a questionnaire that establishes three O behavioral categories: morning type, neither type, and evening type) (Adan & Almirall, 1991). Sleep patterns were monitored for 2 weeks prior to the commencement of the study by use of sleep diaries. We observed no shift or change in bedtime or wake-up time during this initial monitoring period. The student participants were on their summer break, so did not have any classes. No participant was employed during the study period. All volunteers were interviewed and assessed by a sleep specialist to ensure that they did not have sleep complaints. Information about the time and frequency of meals was collected on daily basis. We defined major meals as daily meals that included more that one food and a beverage and the participants had the option to name more than one meal as a major meal (Oltersdorf, Schlettwein-gsell, & Winkler, 1999). Informed consent was obtained from all participants and the protocol was approved by the Ethics Committee of our institute. One of the participants was subsequently excluded as his armband did not collect data during the baseline period. Study protocol Before starting the study, participants reported to the Sleep Disorders Center (SDC) where age, height, weight, and vital signs were recorded and each subject was given training and orientation. According to the manufacturer’s instructions, each participant was asked to wear a SenseWear armband on the triceps of his right arm, over the triceps muscle, at the midpoint between the acromion and olecranon processes. The armband was removed only during swimming and showering. Participants reported to the SDC twice during the study period to download data and charge batteries. Armband The SenseWear Pro ArmbandTM (Body Media, Pittsburgh, PA) is a portable sensing device 8.8 cm 5.6 cm 2.1 cm in size and 82 g in weight. The device measures skin temperature, galvanic skin response, heat flux, and body acceleration (movement). Additionally, the device places the above-measured parameters and descriptive characteristics of the participant (gender, age, height, weight) into proprietary algorithms that report total and active energy expenditure, metabolic equivalent (METS), duration and quantification of physical activity, body position, sleep efficiency, and sleep duration. Technical characteristics of the Armband have been described previously (Dorminy, Choi, Akohoue, Chen, & Buchowski, 2008).
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Accelerometry is measured using a two-axis micro-electronic mechanical sensor. Heat flux is assessed employing a proprietary sensor that incorporates thermal-resistant materials and thermocouple arrays. Galvanic skin response is used as an indicator of evaporative heat loss and is measured using two hypoallergenic stainless steel electrodes. Skin temperature is assessed using a thermistor-based sensor. The measured skin temperature is continuously and linearly indicative of core activities in the body (Teller, 2004). Data provided by the manufacturer showed that skin temperature sensor accuracy was at 0.1 8C in the interval 0– 70 8C. The sensor was calibrated at room temperature (23–25 8C) and these data was stored for offset correction on a scale of 0–50 8C and a resolution of 0.018 8C per A/D tick. Proximal skin temperature follows the same circadian rhythm as does rectal temperature (Krauchi & Wirz-Justice, 1994). The near-body temperature sensor measured the temperature of the cover on the side of the armband and provided information on total energy expenditure. Each sensor was monitored 32 times per second, and data tracked over a period of 1 min (Teller, 2004). Minute-by-minute data from the Armbands were analyzed by algorithms using Body Media1 InnerView1 Research Software (version 5.1) provided by BodyMedia, Inc. (Malvolti et al., 2005). The commercial energy expenditure algorithm was validated by use of double-labeled water (Mignault, St Onge, Karelis, Allison, & Rabasa-Lhoret, 2005) and metabolic carts (Jakicic et al., 2004; Malavolti et al., 2007). In addition, the SenseWear Armband has been validated for study of sleep patterns, as the internal body media algorithm can identify sleep and wakefulness with moderate-to-high sensitivity, specificity, and accuracy (Miwa, Sasahara, & Matsui, 2007; Teller, 2004). The American Academy of Sleep Medicine (AASM) has indicated that actigraphy (the use of devices that monitor body movements) can be a useful adjunct in the diagnosis of circadian rhythm disorders (Littner et al., 2005). ‘‘Total Sleep Time’’ (TST) was defined as the main consolidated sleep period and ‘‘Nap’’ as any other brief period of sleep. Statistical analysis Data in the form of MS Excel spreadsheets were downloaded from each ArmbandTM using Body Media1 ‘‘InnerView1 Professional 5.1. Data for each subject was analyzed individually. For heat flux, skin temperature, near-body temperature, energy expenditure, and METS, data were analyzed and averages were calculated as follows: overall weekly average, overall hourly average for each day, and hourly average for each week. We developed a 24 hcosinor model ( f ðtÞ ¼ M þ A Cosðð2pt=TÞ þ ? Þ; where M = Mesor; A = Amplitude; Ø = Acrophase; T = 24 h) to get the best estimates of the overall acrophase for Skin Temperature and Energy Expenditure. The model was executed for each subject’s data during the three periods. Data was expressed as means SD. Comparisons among BL, R1, and R2 were performed using one-way repeated-measures ANOVA for all variables. Results were considered statistically significant if p values were 0.05. When the difference was significant, post hoc testing was performed using pairwise comparison. Effect size was calculated using partial eta-squared test. Effect size was considered large if the value was .14 (Cohen, 1992). All the participants named one meal per day as a major meal, hence, we named that meal ‘‘the main meal’’ in the results. Standard statistical software (SPSS Version 16.0; SPSS Inc. Chicago, IL) was used for all statistical analysis. Results The mean age of participants was 20.5 2.9 years and the mean body mass index (BMI) was 22.6 2.7 kg/m2. There were no significant changes in BMI throughout the study. Table 1 shows data
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Table 1 Comparison between baseline (BL), and first (R1) and second (R2) weeks of Ramadan. Variable
BL
R1
R2
Number of meals per day Time of the main meal (24 h) Bed time (24 h) Wake time (24 h) TST (h) NAP duration (h) TST + NAP (h) Time of NAP (24 h) Heat flux
2.27 0.82 21.60 1.14 4.0 1.4 10.42 1.87 6.42 1.27 1.61 0.77 7.88 1.19 13.42 1.82 63.76 6.88
2.33 0.52 20.00 2.74 5.6 1.3 12.68 1.41Ü 7.08 0.57 2.08 0.88 9.01 0.91 14.41 1.51 63.9 9.4
2.50 0.55 19.50 2.81 5.42 2.6 11.76 2.32 6.34 0.75 1.94 0.53 8.13 1.07 14.12 0.56 63.9 9.4
Skin temperature (8C) Mesor Amplitude *Acrophase (24 h)
33.14 0.34 0.84 0.67 20.43 1.67
33.22 0.33 0.60 0.71 22.24 1.25
33.24 0.2 0.69 0.73 22.93 1.55
Energy expenditure (kcal/min) *Mesor Amplitude *Acrophase (24 h) *METS
2.28 0.36 1.01 0.38 20.34 1.77 1.88 0.22
2.11 0.35Ü 0.92 0.36 22.38 1.37Ü 1.74 0.16Ü
2.13 0.28 0.85 0.30 22.22 1.73Ü 1.75 0.15
BL: baseline; R1: first week of Ramadan; R2: second week of Ramadan; TST: total sleep time; METS: metabolic equivalent. * P < 0.05 based on repeated measured ANOVA (overall group differences). Ü The difference is statistically significant compared to baseline (p < 0.05) when paired wise comparison were made.
collected during BL, R1, and R2. There were no significant differences in the number of meals or the timing of the main meal between BL and Ramadan. During BL, the participants inconsistently took light meals after awakening (11.25 1.3) and between 02:00 and 03:00 AM (2.6 0.9). During Ramadan, all the participants took a light meal at sunset (time of sunset ranged from 05:59 to 06:21 depending on the date of the month) to break their fast, which consists of a few dates and a drink of water or juice and inconsistently took a light meal (Suhur) before Dawn between 02:00 and 03:45 AM (R1: 2.8 0.5 and R2: 2.9 0.4) (dawn occurred between 04:05 and 04:21 depending on the date of the month). The partial eta-squared statistics indicated large size effect for the delay in bedtime during Ramadan (.27). Wakeup time was delayed during Ramadan (R1 and R2) compared to BL. The difference between BL and R1 was statistically significant (10.42 1.87 vs. 12.68 1.41). Whereas TST was comparable during the three periods, TST + nap time was longer during Ramadan than in BL with a large effect size as indicated by partial eta-squared statistics (.33). Energy expenditure and METS were significantly lowered during Ramadan. There was delay in the acrophase of skin temperature during Ramadan, compared to BL. In other words, there was a shift in the circadian pattern of body temperature during Ramadan. Additionally, there was a delay in the acrophase of energy expenditure during Ramadan. Discussion The current study demonstrated that the major sleep period was delayed as evidenced by a marginally significant delay of bedtime (large effect size) and significant delay of wake-up time, during Ramadan. Additionally, temperature acrophase (i.e., the times at which the maximum values occurred in the circadian cycle), and maximum energy expenditure were delayed. Importantly, our study subjects were young men who did not greatly change their eating habits during Ramadan. These results support our hypothesis that factors other than fasting, such as cultural and lifestyle changes, may cause a shift in the circadian pattern. Previous studies have suggested that a delay in the circadian pattern and a change in chronotype during Ramadan (BaHammam, 2005; Roky et al., 2001). However, most previous studies enrolled
subjects who were working during the day or attending classes and made significant changes to eating habits during Ramadan. None of our subjects had daytime commitments and all had an eveningtype chronotype, thus minimizing the effect of changing the timing of meals. Additionally, previous studies did not control for the practice used in some Muslim countries of delaying the starting time of work and schools by 2–3 h during Ramadan (BaHammam, 2006). It is known that delays in wake-up time can delay circadian phase significantly and hence temperature rhythm (Taylor, Wright, & Lack, 2008). Our studied subjects had no daytime commitments during the study period and their bedtime and wake-up times were stable for 2 weeks during the baseline period prior to the beginning of the study. A study assessed the chronotype of fasting and non-fasting individuals during Ramadan in Saudi Arabia using an abridged ¨ stberg questionnaire (morningness/ version of the Horne and O eveningness test) (BaHammam, 2005). Interestingly, a change in chronotype was seen in non-fasting non-Muslim residents during Ramadan, with an increase in neither-types and a decrease in morning-types at the beginning and end of Ramadan suggesting that factors other than changes in meals timing may be involved (BaHammam, 2005). Previous studies have monitored body temperature as a marker of circadian pattern during Ramadan (BaHammam, 2004; Roky et al., 2001; Roky, Iraki, HajKhlifa, Lakhdar Ghazal, & Hakkou, 2000). In general, body temperature falls during sleep and rises at wake time. Roky and associates monitored rectal temperature for 24 h in a sample of fasting individuals during Ramadan (Roky et al., 2001). The cited authors reported a delay in the occurrence of acrophase and a reduction in the amplitude of core body temperature during Ramadan. Another study which measured oral temperature confirmed these results. This latter study showed a significant rise in body temperature at 23:00 and 00:00 h and a significant reduction at 09:00, 11:00, 13:00, and 16:00 h (Roky et al., 2000). However, a third study found no significant change in the circadian pattern of oral temperature at 08:00, 16:00, and 00:00 h during the first and third weeks of Ramadan (BaHammam, 2004). Levels of the hormone melatonin also provide a reliable and reproducible marker of circadian changes in humans (Arendt, 1995). Two studies found that a smaller delayed night peak and a flatter slope of serum concentration of melatonin during Ramadan (BaHammam, 2004; Bogdan, Bouchareb, & Touitou, 2001). To the best of our knowledge, no study has previously examined the circadian pattern of energy expenditure during Ramadan. However, examinations of the circadian pattern of energy expenditure in humans have yielded conflicting results. In one study, Consoli and co-workers examined the effect of different meal times on the circadian pattern of energy expenditure in 15 subjects, by measurement of O2 consumption and CO2 production (Consoli et al., 1981). These authors concluded that meal-time did not affect the circadian rhythm of energy expenditure and suggested that the rhythm is endogenous. In our subjects, there was a delay in the peak of energy expenditure, of about 2 h, during R1 compared to BL. This delay continued during the second week of Ramadan and coincided with our measured changes in skin temperature. In general, exercise is best tolerated when the resting body temperature is highest (Atkinson & Reilly, 1996). Thus, we observed a delay in energy expenditure even though eating time did not change significantly during the study period. The current study demonstrated rapid changes in bedtime and wake-up time during Ramadan, in agreement with previous work (BaHammam, 2003, 2005; Roky et al., 2001). Such obvious changes reported in previous studies may be partially explained by delays in starting work during Ramadan (BaHammam, 2006). Nevertheless, a delay in bedtime during Ramadan also occurred in nonfasting residents of Saudi Arabia whose work commencement time
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did not change (BaHammam, 2005). This supports our hypothesis that lifestyle changes other than fasting may cause a shift in circadian pattern during Ramadan (BaHammam, 2005). Data on sleep duration during Ramadan varies with country and these differences seem to be related to lifestyle and cultural differences (BaHammam, 2006). In a sample of university students in Morocco, night-time sleep duration decreased significantly during Ramadan (Taoudi Benchekroun, Roky, Toufiq, Benaji, & Hakkou, 1999). Another study in the United Arab Emirates reported a decrease in night-time sleep duration in university students, but this was compensated by daytime naps (Margolis & Reed, 2004). On the other hand, studies in Saudi Arabia reported no difference in night-time sleep duration or total sleep time (nighttime + naps) during Ramadan (BaHammam, 2003, 2005). The present study, which enrolled Saudi students, is in agreement with the above two studies concerning the role of lifestyle and cultural differences on changes in circadian patterns during Ramadan. The current study has some limitations that need to be addressed. First, the number of recruited volunteers is relatively low. Nevertheless, this limitation is inherent to studies like this that use objective assessment within a short specified period (BaHammam, 2004; Roky et al., 2003; Roky et al., 2001). A larger sample would be necessary to identify predictors of circadian rhythm delay during Ramadan. Second, despite the fact that we recruited volunteers with DSPS to ameliorate the sudden shift in the circadian pattern of caloric intake, the time of meals during BL did not coincide precisely with the time of meals during R1 and R2. However, the timing of the main meal was not significantly different during the three periods and the results did demonstrate a shift in the acrophase of temperature. In summary, we used a validated portable device to measure sleep pattern, skin temperature, and energy expenditure in a small group of young healthy men with evening chronotypes who did not significantly change their eating habits during Ramadan. With the onset of Ramadan, we observed clear delays in bedtime and wake-up time, and in the circadian rhythms of skin temperature and energy expenditure. These findings support our hypothesis that factors other than fasting and mealtime can affect sleep patterns and circadian rhythms during Ramadan. We suggest that future studies seek to identify these factors and monitor the same physiological parameters in fasting and non-fasting individuals during Ramadan. Acknowledgements This project was supported by a grant from the University Sleep Disorders Center of King Saud University and King Abdulaziz City for Science and Technology. The authors would like to thank Dr. Shaffi Shaikh from the Department of Family Medicine, King Saud University for the statistical review. References ¨ stberg morningness–eveningness questionAdan, A., & Almirall, H. (1991). Horne & O naire: a reduced scale. Personality and Individual Differences, 12, 241–253. Arendt, J. (1995). Melatonin and the Mammalian Pineal Gland. London, UK: Chapman & Hall.
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