J Relig Health (2014) 53:929–942 DOI 10.1007/s10943-013-9687-0 ORIGINAL PAPER
Does Ramadan Fasting Alter Body Weight and Blood Lipids and Fasting Blood Glucose in a Healthy Population? A Meta-analysis ¨ ztu¨rk • Gu¨lendam Karadag˘ Seval Kul • Esen Savas¸ • Zeynel Abidin O
Published online: 20 February 2013 Ó Springer Science+Business Media New York 2013
Abstract In this study, we conducted a meta-analysis of self-controlled cohort studies comparing body weights, blood levels of lipids and fasting blood glucose levels before and after Ramadan taking into account gender differences. Several databases were searched up to June 2012 for studies showing an effect of Ramadan fasting in healthy subjects, yielding 30 articles. The primary finding of this meta-analysis was that after Ramadan fasting, lowdensity lipoprotein (SMD = -1.67, 95 % CI = -2.48 to -0.86) and fasting blood glucose levels (SMD = -1.10, 95 % CI = -1.62 to -0.58) were decreased in both sex groups and also in the entire group compared to levels prior to Ramadan. In addition, in the female subgroup, body weight (SMD = -0.04, 95 % CI = -0.20, 0.12), total cholesterol (SMD = 0.05, 95 % CI = -0.51 to 0.60), and triglyceride levels (SMD = 0.03, 95 % CI = -0.31, 0.36) remained unchanged, while HDL levels (SMD = 0.86, 95 % CI = 0.11 to 1.61, p = 0.03) were increased. In males, Ramadan fasting resulted in weight loss (SMD = -0.24, 95 % CI = -0.36, -0.12, p = 0.001). Also, a substantial reduction in total cholesterol (SMD = -0.44, 95 % CI = -0.77 to -0.11) and LDL levels (SMD = -2.22, 95 % CI = -3.47 to -0.96) and a small decrease in triglyceride levels (SMD = -0.35, 95 % CI = -0.67 to -0.02) were observed in males. In conclusion, by looking at this data, it is evident that Ramadan fasting can effectively change body weight Electronic supplementary material The online version of this article (doi:10.1007/s10943-013-9687-0) contains supplementary material, which is available to authorized users. S. Kul Department of Biostatistics, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey E. Savas¸ (&) Department of Internal Medicine, Subdivision of Social Medicine, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey e-mail:
[email protected] ¨ ztu¨rk Z. A. O Department of Internal Medicine, Subdivision of Geriatrics, Faculty of Medicine, University of Gaziantep, Gaziantep, Turkey G. Karadag˘ Department of Publich Health-Nursing School, University of Gaziantep, Gaziantep, Turkey
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and some biochemical parameters in healthy subjects especially in males compared to preRamadan period. Keywords Ramadan Fasting Body weight Lipid profile Triglyceride Blood glucose levels Abbreviations HDL High-density lipoprotein (HDL) LDL Low-density lipoprotein RFR Ramadan fasting RCT Randomized controlled trial SMD Standardized weighted mean difference
Introduction It is estimated that currently there are more than 1.5 billion Muslims in the world. Most of them reside in Asia (69 %) and Africa (27 %) (Kettani 2010). Because Islam is accepted as a way of life by Muslims, most of the Muslims live according to Islamic rules. One of the Islamic rules for Muslims is fasting during Ramadan. Fasting is normally defined as abstinence from some or all food, liquid, or both for a defined period of time. There are various fasting rituals with a distinct content and practicing ways in different religions (Trepanowski and Bloomer 2010). While Jews fast 6 days of the year, the fasting period for Greek Orthodox Christians is 180–200 days each year. Ramadan, the ninth lunar month of the Islamic calendar, is a holy month in Islam and lasts for 28–30 days. In Ramadan period, fasting is an obligatory practice for all Muslims except for pregnancy, lactation or menstruation in women, or any illness in both men and women. Every year most of the Muslims fast during the holy month of Ramadan. Duration of Ramadan fasting varies between countries and seasons, with an average length of 12–16 h. During this period, Muslims who fast are allowed to eat and drink only from sunset to sunrise. Muslims enjoy a feasting atmosphere at sunset and consume many different kinds and large amount of foods and drinks freely. Only foods and drinks which are forbidden by the religion are the main dietary restrictions in this feast. Eating within a short overnight span not only impairs feeding schedule but also affects sleep duration (Iraki et al. 1997). Because Ramadan fasting affects a huge population, numerous studies were performed in the last two decades to show the effect of Ramadan fasting on various parameters in healthy (Dewanti et al. 2006; Ziaee et al. 2006) and unhealthy populations (Khafaji et al. 2012; Sadiya et al. 2011; Savas et al. 2012). In most of the studies, it was found that Ramadan fasting leads to changes in the metabolic status including blood glucose, lipid profile, hematological parameters, and body weight (Dewanti et al. 2006; Khafaji et al. 2012; Sadiya et al. 2011; Savas et al.2012; Ziaee et al. 2006). However, results of these studies vary due to eating habits, gender, age, and ethnicity. For this reason, we conducted a contemporary meta-analysis including all recent studies on healthy subjects with normal body weight to show the effect of Ramadan fasting on the most widely reported health outcomes including body weight, total cholesterol, HDL, LDL, triglycerides, and fasting blood glucose.
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Methods Literature Search We used the Cochrane Handbook for Systematic Reviews of Interventions. A systematic review protocol was developed and a search was conducted in Medline, Cinahl, and EMBASE with no time limit. The search strategies combined key subject terms and words, and search filters were validated. More details about search strategies are given in the supplementary file.
Study Inclusion/Exclusion Criteria We included before–after studies and interrupted time series in the meta-analysis. All the included studies compared the outcomes before and after Ramadan fasting. Studies were included when at least one of the following outcome indicators has been evaluated: body weight, total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), and triglycerides and fasting blood glucose. Only studies that enrolled healthy participants or participants with normal body weight were included. Articles that were strictly descriptive (study protocols, review articles, and theoretical articles), articles on nonhealthy, pregnant, and obese subjects, articles with an experimental design such as dietary plans and exercising, and articles that did not assess at least one of the six aforementioned outcomes were excluded. Only studies in English were included. Studies were eligible if participants were adults (aged 18 years and over).
Outcome Measures In this study, results were combined according to six outcome indicators: body weight, total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides, and fasting blood glucose. Among the included studies, these were the most commonly used outcomes for which results were available.
Data Extraction and Quality Assessment Author, publication year, sample size, characteristics of the population studied (age, sex, race, geographical location, etc.), and outcome measures were recorded. Two reviewers independently screened the titles, abstracts, and keywords to identify eligibility and assessed methodological quality of the included studies and recorded the findings. The reviewers were blinded to the names of the authors, the institution where the study had been carried out, and the journal. Any disagreement was discussed with a third reviewer. Assessment of the methodological quality of the included studies was based on the New Castle Ottawa Scale. All the studies meeting the inclusion criteria (see above) with any items of the checklists were excluded. For continuous variables, means and standard deviations were used. If an article only reported standard error instead of standard deviation, standard deviations were calculated via formula connection between them (SE = SD/sqrt(n)).
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Data Analysis Data analyses were performed by the guidelines regarding statistical methods as set out by The Cochrane Collaboration (Higgins and Green 2011). We used random effect models to conduct meta-analyses of continuous outcomes to eliminate the effect of heterogeneity on results for all the outcomes (Higgins et al. 2003). Sensitivity analysis was performed to identify studies with a poor quality (Leandro and Gallus 2003). For each outcome, metaanalyses were repeated many times to check the robustness of findings using different assumptions. The largest, the smallest, the earliest studies, and studies with the most contradictory results were excluded, respectively, to see how they affected the metaanalysis when they were included. Results of the sensitivity analysis are given in the supplementary file. In addition to the sensitivity analysis, potential publication bias was assessed using a funnel plot which is a scatter plot of the estimate of effect from each study in the meta-analysis against a measure of its precision, usually 1/SE (See, supplementary file). Results for each measured outcome are presented separately for different study types. The results are presented with the Forest plot, which showed the strength of the evidence: In the plot, the left-hand column lists the names of the studies; the right-hand column shows the measure of effect (expressed as SMD with 95 % CI). According to the test, the overall meta-analyses were considered as not having any statistically significant effects at the given level of confidence when the overall diamonds overlapped the line of no-effect results. SMD smaller than 0.40 is interpreted as a small effect size, SMD between 0.40 and 0.70 as moderate, and [0.70 as a large effect size (Higgins and Green 2011). Analyses were performed using Review manager software (RevMan), version 5.0, and a p value \0.05 was considered statistically significant.
Results Description of the Studies The search strategy identified a total of 14,120 records. Among 146 studies identified, 30 publications met the study inclusion criteria and they were included in the meta-analysis for a total sample of 1,476 healthy subjects (923 men, 553 women), as shown in PRISMA flow diagram in Fig. 1. This meta-analysis consists of thirty self-controlled (before-after Ramadan) cohort studies. Fifteen of the studies have enrolled only male participants and 5 studies have been conducted only in women. Ten studies have enrolled both women and men. A summary of study characteristics is given in the supplementary file. Seven studies were performed in Iran, four in Jordan, and three in Turkey. The study setting characteristics (urban/rural typology, education, living conditions) were not fully reported. Effect of Ramadan Fasting: Body Weight Twenty-one studies were included in the meta-analysis to estimate the pooled reduction in body weight after Ramadan fasting compared with before Ramadan fasting. A total of 830 participants were analyzed, including 531 participants in the male subgroup and 299 participants in the female subgroup. Ramadan fasting had a small significant positive effect in men (SMD = -0.24 [-0.36, -0.12], p = 0.001), but no significant difference was observed among women (SMD = -0.04 [-0.20, 0.12], p = 0.620). The overall pooled
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Fig. 1 PRISMA flow diagram of search results
SMD for body weight was -0.17, 95 % CI = -0.26 to -0.07, which was significant (p = 0.001). SMD estimates and their 95 % confidence intervals are shown in Fig. 2. There was no heterogeneity across studies for weight loss (I2 = 0 %, p = 0.82). Effect of Ramadan Fasting: Total Cholesterol We included in the meta-analysis 20 studies reporting estimates for total cholesterol. A total of 806 participants were analyzed, including 581 participants in the male subgroup and 225 participants in the female subgroup. Figure 3 displays the result of the metaanalysis. The overall results for males and females were SMD -0.44, 95 % CI = -0.77 to
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Fig. 2 Forest plot for pre–post-Ramadan changes in body weight
-0.11, p = 0.009; and SMD = 0.05, 95 % CI = -0.51 to 0.60, p = 0.870, respectively, and the overall result of meta-analysis was significant (SMD = -0.29, 95 % CI = -0.57 to 0.00, p = 0.050). There was heterogeneity across studies for total cholesterol (I2 = 86 %, p = 0.001). Effect of Ramadan Fasting: High-density Lipoproteins (HDL) A total of 13 studies provided data for the meta-analysis for HDL change (661 participants; 462 men and 199 women). In the subgroup analysis, men showed no significant difference (SMD = 0.63, 95 % CI = -0.67 to 1.92, p = 0.34), but there was a large significant change in HDL scores of women (SMD = 0.86, 95 % CI = 0.11 to 1.61, p = 0.030). The overall results of random effect model showed that Ramadan fasting does not lead to any significant changes in HDL levels (SMD = 0.73, 95 % CI = -0.10 to 1.57, p = 0.090) (Fig. 4). There was heterogeneity across studies for HDL (I2 = 98 %, p = 0.001). Effect of Ramadan Fasting: Low-density Lipoproteins (LDL) Thirteen of the included studies representing a healthy population of 740 participants (500 men, 240 women) reported LDL scores before and after Ramadan fasting. Overall metaanalysis results of the random effect model showed a large significant reduction in LDL levels compared to pre-Ramadan levels as shown in Fig. 5 (SMD = -1.67,
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Fig. 3 Forest plot for pre–post-Ramadan changes in total cholesterol
95 % CI = -2.48 to -0.86, p = 0.001). Also, the subgroup analysis showed similar results (men; SMD = -2.22, 95 % CI = -3.47 to -0.96, p = 0.001, women; SMD = 0.81, 95 % CI = -1.61 to -0.00, p = 0.050), and test for subgroup differences showed no significant difference (p = 0.06). There was heterogeneity across studies for LDL (I2 = 98 %, p = 0.001). Effect of Ramadan Fasting: Triglycerides Nineteen studies were included in the meta-analysis to estimate the pooled changes in triglycerides after Ramadan fasting compared with before Ramadan fasting. A total of 828 participants were analyzed, including 538 participants in the male subgroup and 290 participants in the female subgroup. Ramadan fasting had a small significant positive effect in men (SMD = -0.35 [- 0.67, -0.02], p = 0.040), but no significant difference was observed in women (SMD = -0.03 [- 0.31, 0.36], p = 0.880). The overall pooled SMD for triglycerides was -0.20 (95 % CI = -0.44 to 0.04, p = 0.100). SMD estimates and their 95 % confidence intervals are shown in Fig. 6. There was heterogeneity across studies for triglycerides (I2 = 82 %, p = 0.001). Effect of Ramadan Fasting: Fasting Blood Glucose (FBG) We included in the meta-analysis 16 studies reporting estimates for fasting blood glucose. A total of 776 participants were analyzed, including 611 participant in the male subgroup
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Fig. 4 Forest plot for pre–post-Ramadan changes in HDL
Fig. 5 Forest plot for pre–post-Ramadan changes in LDL
and 165 participants in the female subgroup. Figure 7 displays the result of the metaanalysis. SMD for men was -1.11 (95 % CI = -1.72 to -0.49, p = 0.001). Results for women included SMD was -1.09 (95 % CI = -2.11 to -0.06, p = 0.040). The overall
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Fig. 6 Forest plot for pre–post-Ramadan changes in triglycerides
pooled SMD for FBG was -1.10 (95 % CI = -1.62 to -0.58, p = 0.001). Test for subgroup differences showed no significant difference (p = 0.97). There was heterogeneity across studies for triglycerides (I2 = 95 %, p = 0.001).
Discussion We performed a meta-analysis to evaluate the effect of Ramadan fasting on a number of health outcomes including body weight, total cholesterol, HDL, LDL, triglycerides, and fasting blood glucose. To the best of our knowledge, this study is the first meta-analysis to show an effect of Ramadan fasting on the healthy people. The primary finding of this meta-analysis was that after Ramadan fasting, LDL and FBG levels decreased in both sex groups and in the overall group compared to levels before Ramadan. Additionally, while there was no change in the body weight, total cholesterol, and triglyceride levels in the female subgroup, HDL levels were increased. On the other hand, Ramadan fasting resulted in weight loss among men. Also a large reduction in total cholesterol and LDL levels and a small decrease in triglyceride levels were observed in males. Unlike women, no changes were observed in HDL levels. By looking at this data, it is evident that Ramadan fasting can effectively change body weight and some biochemical parameters compared to pre-Ramadan levels of participants. During the Ramadan fast, Muslims eat two meals a day, one before the sunrise and the other shortly after sunset. During Ramadan, most Muslims change their lifestyle (Toda and Morimoto 2000), sleep hours (Bahammam 2006), physical activities
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Fig. 7 Forest plot of pre–post-Ramadan change in fasting blood glucose
(Chaouachi et al. 2009), food consumption, frequency of meals, and dietary patterns for different reasons (Trepanowski and Bloomer 2010; Azizi 2010; Yakoob 2006; Guerrero et al. 2009; Afifi 1997). The general opinion is that fasting has a potential non-pharmacological intervention for improving health and increasing longevity (Azizi 2010). While religious fasting is often a time of great spiritual growth, it can also be a time of great improvement to one’s physical health. During the holy month of Ramadan, there is a change in feeding pattern in which larger meals compensated for lower frequency of food ingestion. Previous research indicated that despite insignificant changes in the total energy intake, a significant reduction was found in total body weight. It may be argued that weight loss is partly attributed to efficient utilization of body fat during Ramadan fasting (El Ati et al. 1995; Hallak and Nomani 1988; Husain et al. 1987; Nomani et al. 1990; Sliman and Al-Khatib 1988; Takruri 1989; Nomani et al. 1992; Athar and Habib 1994). Animal studies found that eating one meal each day resulted in weight loss and a decrease in fat mass with little modification in calorie intake (Stote et al. 2007; Trepanowski et al. 2011). It has been established that a given nutrient ingested at an unusual time can induce different metabolic effects (Lamine et al. 2006). Hormones which are related to the energy metabolism and the regulation of energy intake should affect body weight (Kassab et al. 2004; Bogdan et al. 2001). When we reviewed the meta-analysis results in terms of health benefits of Ramadan, we observed that body weight was decreased in the general population and males. Most of the women in Muslim society are housewives who do not work outside, so their physical activities are less than men during Ramadan. However, men continue their daily routines and activities. For this reason, a significant weight loss might be observed in males. Another finding of our meta-analysis was that there was a statistically significant reduction in total cholesterol and triglycerides in males and a significant reduction in LDL
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levels in both males and females. However, HDL levels increased significantly only among women. It was suggested that eating one large meal each day (binge eating) leads to a significant increase in serum HDL levels, while decreasing the LDL/HDL ratio in healthy subjects during Ramadan (Maislos et al. 1993; Streja et al. 1980; Murphy et al. 1996) Furthermore, it is known that the lipid profile is influenced by dietary habits, physical factors, the percentage of fat, type of fat saturation, and the percentage of simple sugars in the daily diet and weight loss (Tsai et al. 2003; Maislos et al.1993; Nagra et al. 1998; Hallak and Nomani 1988; Adlouni et al. 1997; Nomani et al. 1992; Nomani 1997; Furuncuoglu et al. 2007). In addition, smoking is forbidden during the daylight hours of Ramadan; therefore, a human population consisting of a large number of smokers could conceivably experience changes in health-related biomarkers simply by virtue of smoking less. Smoking is limited to nighttime only. Thus, reducing the number of cigarettes may result in positive changes in lipid profiles. In this study, we observed a statistically significant reduction in glucose levels in both males and females. During Ramadan fasting, the sleep–wakefulness cycle is also altered. This leads to changes in the levels of leptin, neuropeptide-Y, and insulin, all playing an important role in the long-term regulation of energy intake and energy expenditure (Kassab et al. 2004). Also, it has been shown that alterations in sleep patterns and psychological/ social habits during Ramadan induce changes in the rhythmic pattern of a number of hormonal variables, that is, melatonin, steroid hormones (cortisol, testosterone), pituitary hormones (prolactin, luteinizing hormone, follicular stimulating hormone, growth hormone, and thyroid-stimulating hormone), and thyroid hormones (Bogdan et al. 2001). These hormones are related to energy metabolism and regulation of energy intake (Kassab et al. 2004; Bogdan et al. 2001). These hormonal changes could explain decreases in blood glucose levels. In this meta-analysis, we only included studies on healthy participants with normal body weight. However, there are considerable number of studies which showed the effect of Ramadan fasting on diabetes, chronic heart diseases, and obesity. Apart from the nonhealthy population, there are some studies showing the effect of Ramadan fasting on physical exercising and performance of athletes. Also, there are a number of previously performed generic systematic reviews, some of which included patients with chronic conditions and others not providing a primary meta-analysis (Maughan et al. 2010; Azizi 2010: Trepanowski and Bloomer 2010). This systematic review has some limitations. It is known that a meta-analysis of wellconducted randomized controlled trials is the most rigorous way to show the best evidence. But Ramadan fasting is an act of willing abstinence, and only observational studies were performed to show an effect of Ramadan fasting on health outcomes. Therefore, in this meta-analysis, only self-controlled cohort studies were included. Most of the studies were well-balanced with respect to mean age. Sensitivity analysis was performed to identify studies with a poor quality, and for all of the outcomes, the effect size was very similar in this sensitivity analysis (supplementary file 1). Although we included all studies which met our inclusion criteria, most of the participants were men (62.5 %). Sex ratio (male/female) of the participants was 1.67. To reduce the effects of gender and unbalanced sample size on outcome estimations, a subgroup analysis was done and discussed. Also, most of the studies had a relatively small sample size. Another limitation of our study was that despite conducting a search from 1950 to 2012, we could not identify any eligible study up to 1978. And only 6 of the included studies were performed before 2000. Thus, we can conclude that our study results are valid for the last 12 years.
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Conclusion Our purpose was to demonstrate the impact of Ramadan fasting on a number of health outcomes. We observed a significant weight loss both in men and in the overall group, but no such significant changes in women. Also, significant decreases were observed in total cholesterol and LDL levels. By combining all results of studies, it can be concluded that Ramadan fasting leads to decreased LDL levels, but no increases in HDL and triglycerides. FBG levels were also significantly reduced after Ramadan fasting. The findings of this meta-analysis show that Ramadan fasting has some positive effects on a number of health outcomes in a healthy Muslim population, especially among men. However, one should consider limitations of this study while interpreting the results. In future, this meta-analysis should be updated to increase the number of female participants. More investigations are necessary to show sustainability of this positive effect. Also, a meta-analysis is needed to show the effect of Ramadan fasting on health outcomes in people with chronic conditions, especially diabetes and obesity. Conflict of interest The authors declare that they have no competing interests.
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