Effects of Ramadan Fasting on Biochemical and ...

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Effects of Ramadan Fasting on Biochemical and Hematological Parameters and Cytokines in Healthy and Obese Individuals Article in Metabolic syndrome and related disorders · April 2011 DOI: 10.1089/met.2010.0084 · Source: PubMed

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METABOLIC SYNDROME AND RELATED DISORDERS Volume 9, Number 2, 2011 ª Mary Ann Liebert, Inc. Pp. 157–161 DOI: 10.1089/met.2010.0084

Effects of Ramadan Fasting on Biochemical and Hematological Parameters and Cytokines in Healthy and Obese Individuals ¨ nalacak, M.D.,1 ˙Ismail Hamdi Kara, M.D.,2 Davut Baltaci, M.D.,2 Murat U ¨ zgu¨r Erdem, M.D.,3 and P. Gamze Erten Bucaktepe, M.D. 4 O

Abstract Background: The typical nutritional plan in Ramadan may have beneficial influences on the inflammatory state, as well as on metabolic and anthropometric parameters. We aimed to investigate the effects of Ramadan fasting on biochemical and hematological parameters and cytokines in healthy and obese individuals. Methods: This study was performed during the Ramadan holy month (September and October 2007). The study group consisted of 10 obese males and the control group consisted of 10 males with a normal body mass index (BMI), who were admitted to the Family Medicine Outpatient Clinic of Dicle University Medical Faculty in Diyarbakir, Turkey, and who indicated that they were going to fast throughout the entire month of Ramadan. Individuals with any acute or chronic disease or medication during the study were excluded. Height, weight, BMI, and waist and hip circumferences were measured. High-density lipoprotein cholesterol (HDL-C) and lowdensity lipoprotein cholesterol (LDL-C), triglyceride (TG), urea, creatinine, insulin, total protein, albumin, C-reactive protein (CRP), lactic dehydrogenase (LDH), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and cytokine levels were evaluated. Results: The average age of the participants was 27.4 5.2 years. Of the study group, 7 fulfilled the criteria of metabolic syndrome. Significant weight reduction, significant decrease in BMI, and significant decrease of homeostasis model assessment of insulin resistance (HOMA-IR) and fasting blood glucose (FBG) were observed in study group; weight and BMI reduction were insignificant and no significant change was observed in FBG levels, but a significant increase was observed in HOMA-IR in the control group. Post-Ramadan systolic and diastolic blood pressure values, serum white blood cells (WBC) count, interleukin-2 (IL–2), IL–8, tumor necrosis factor-a (TNF-a, TG, and ALT levels were significantly lower in both groups compared to pre-Ramadan values. Conclusion: Ramadan fasting has beneficial influences on the inflammatory state, as well as metabolic and anthropometric parameters.

Introduction

O

besity, diabetes mellitus, and metabolic syndrome are known to be associated with alterations in metabolic parameters. Among these, obesity is the most commonly seen metabolic disease. It can be accepted to be an endemic, and its prevalence is increasing all over the world. Measures for treatment and control of obesity must be on the priority list of the health sector. Prevention is through reduced energy intake and active lifestyle. Dietary therapy for obesity is

usually combined with other weight reduction methods. In fasting, there is a constant restriction on the eating schedule that may have an effect on body biochemical and physiological functions.1 Fasting is considered to be a healthy practice in many cultures and religions. Modern laboratory studies have shown a positive effect of fasting on longevity. The Ramadan holy month (Islamic fasting during Ramadan month, the ninth lunar month of the Muslim year) is observed by millions of Muslims all over the world.2 It provides a natural

1

Medical Faculty, Department of Family Medicine, Eskis ¸ ehir Osmangazi University, Eskis ¸ ehir, Turkey. Medical Faculty, Department of Family Medicine, Duzce University, Duzce, Turkey. Lice Halis Toprak Foundation Village Hospital, Lice, Diyarbakır, Turkey. 4 Medical Faculty, Department of Family Medicine, Dicle University, Diyarbakır, Turkey. 2 3

157

¨ NALACAK ET AL. U

158 environment for the epidemiological study of the effects of fasting on human health. During the Ramadan month, frequency and quantity of food and daily physical activity are changed; food and fluid intake are mainly nocturnal. The food habits, as well as food quality, differ during Ramadan fasting compared with other months.3 There is tendency to consume foods that are richer in carbohydrates during this period. The Ramadan month is not fixed within a year; it has its own pattern period due to the Islamic calendar, so the daily period of fasting, which starts with the dawn and ends with the sunset, varies depending on season of the year and geographical location. Thus, depending upon the season and the geographical location of the country, the duration of fasting varies from 12 to 19 h per day.4 All differences during Ramadan can affect the metabolic state and anthropometric measurements of people who fast during Ramadan. It is well known that a given nutrient ingested at an unusual time can induce different metabolic effects. In several studies, it was shown that lipid profile is affected by dietary habits, percentage of fat in the daily diet and its saturation, and amount of exercise.5 Food habits change during Ramadan when Muslims take meals two times a day—‘‘iftar’’ as the evening dinner and ‘‘sahor’’ at the end of the night, just before the dawn. More food and beverages are consumed at dinner in Ramadan, compared to other times. Overall, the total daily amount of food taken during Ramadan decreases. This means that Ramadan fasting is like a diet program. Therefore, it has metabolic, anthropometric, and physiological effects on the human body. In general, body weight is reduced during Ramadan fasting. It has been reported in the literature that the serum high-density lipoprotein cholesterol (HDL-C) level is increased and the low-density lipoprotein cholesterol (LDLC) level is decreased due to Ramadan fasting.6 The bases for potential effects of Ramadan fasting on metabolic and biochemical parameters, as well as anthropometric measurements, are being investigated. There are several studies reporting effects of Ramadan fasting on anthropometric measurements, lipid profile, and some biochemical parameters, such as glucose and renal and liver enzymes.7 However, information regarding effects of Ramadan fasting on level of serum cytokines is scarce. In this study, we investigated the effects of Ramadan fasting on obese individuals’ serum cytokines, inflammatory markers, and insulin resistance, along with lipid profile and anthropometric measurements.

Materials and Methods This cross-sectional and descriptive study was planned by a commission of lecturers from Dicle University (Prof. Ismail Hamdi Kara, now at Duzce University) and Zonguldak Karaelmas University (Assoc. Prof. Murat Unalacak, now at Eskisehir Osmangazi University), and performed during the Ramadan holy month of September and October 2007 (in the Islamic year 1428). The study group consisted of 10 obese males and the control group consisted of 10 males with normal body mass index (BMI), who were admitted to the Family Medicine Outpatient Clinic of Dicle University Medical Faculty in Diyarbakir, Turkey, and who indicated that they were going to fast throughout Ramadan. Exclusion criteria were being female and having type 2 diabetes mellitus, infectious conditions, acromegaly, hypertension, and any addiction or drug therapy. Males were selected for the

study because females are exempt from fasting during their menstrual period. All participants completed a monthly period of Ramadan fasting. All of the patients’ height, weight, and waist and hip circumferences were measured, and BMI was calculated for each. Body weights were measured without shoes and in light clothing, and were recorded to the nearest 0.5 kg. Body heights were measured without shoes or cap, and were recorded to the nearest centimeter. The BMI was expressed as body weight in kilograms divided by square of height in meters. Blood samples were collected in tubes from all subjects before and after Ramadan month. All blood samples were sent to the Central Laboratory of Dicle University Medical Faculty. Serum was separated from samples through centrifugation and assays were completed instantly. The total cholesterol (TC), HDL-C and LDL-C, triglyceride (TG), urea, creatinine, insulin, total protein, albumin, C-reactive protein (CRP), lactic dehydrogenase (LDH), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and cytokine levels were measured. The serum interleukin level was measured, using the chemiluminescence immunoassay method via the Immulite 100 system. Serum insulin levels were measured by radioimmunoassay (RIA; Diagnostic System Laboratories, Webster, TX, Berthold LB 2111). TC (HDL and LDL) and TG levels were determined using the Abbott Aeroset auto analyzer after a 12-h fasting period. The LDL-C was calculated by the Friedewald equation [LDL-C ¼ TC (HDL þ TG/5)]. In our study, mathematical modeling of the fasting glucose and insulin pairs, homeostasis model assessment–insulin resistance index (HOMA-IR) was used as an index of pancreatic b-cell function and tissue insulin sensitivity, and it was calculated using homeostasis model assessment. The subjects having a HOMA-IR value >2.2 were accepted to have insulin resistance. The HOMA-IR was calculated from fasting plasma glucose (FPG) and fasting immunoreactive insulin (FIRI) according to the report by Matthews et al. HOMA-IR ¼ Fasting insulin (mU/mL)fasting glucose (mmol/L)/22.5. The goal was to keep the HDL/LDL ratio above 0.3, with the ideal HDL/LDL ratio being above 0.4. For CRP, a value of 3 mg/L was accepted as the cutoff value. All calculations were done using the SPSS v. 11.5 statistical software package (the system for statistics) for analysis of the data. All data were expressed as mean standard deviation (SD). Comparisons between means observed before and after Ramadan were tested using a paired t-test. The data within each phase were also examined using Pearson r correlation analysis to find the relationship between the studied variables. All differences were considered to be significant at p < 0.05.

Results Twenty consecutive male patients with an average age of 27.4 5.2 were enrolled in the study. Seven patients from the obesity group filled the criteria of metabolic syndrome. After Ramadan fasting, marked weight reduction was observed in the obesity group (83.2 8.4 kg versus 80.3 7.9 kg, p < 0.001), but only light weight reduction was observed in the nonobesity group (71.9 5.9 kg versus 71.1 6.0 kg, p > 0.05). Moreover, BMI was also significantly reduced in obese patients (28.1 2.1 kg/m2 and 27.2 2.0 kg/m2; p < 0.01), whereas it was also, but not significantly, reduced

EFFECTS OF RAMADAN FASTING ON OBESE INDIVIDUALS Table 1.

159

Changes in Anthropometric Measurements, HOMA-IR, FBG, and Blood Pressure in Both Groups According to Pre- and Post-Ramadan Study (n ¼ 10)

Weight BMI FBG Insulin HOMA-IR SBP DBP HDL/LDL

Control (n ¼ 10)

Pre-Ramadan

Post- Ramadan

P

Pre-Ramadan

Post-Ramadan

P

83.2 8.4 28.1 2.1 97.2 13.5 7.6 3.4 1.69 0.82 120 7 79 9 0.44 0.19

80.3 7.9 27.2 2.0 93.0 7.0 6.9 3.3 1.57 0.76 114 8 75 11 0.41 0.16

0.05 >0.05 0.05 >0.05 >0.05 0.05 0.05 >0.05 >0.05 >0.05 >0.05 0.05 0.05 >0.05 0.05 >0.05 >0.05 >0.05 ¼ 0.005 >0.05

27.4 5.9 1.02 0.11 7.7 0.3 4.7 0.3 120 59 170 56 45 5 100 49 19 3 23 9 165 20

26.9 8.5 0.98 0.18 7.7 0.4 4.6 0.3 93 53 168 49 45 4 104 45 20 7 20 13 177 22

>0.05 >0.05 >0.05 >0.05 0.05 >0.05 >0.05 >0.05 >0.05 >0.05

BUN, blood urea nitrogen; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; AST, aspartate aminotransferase; ALT, alanine aminotransferase; LDH, lactate dehydrogenase.

difference between pre-Ramadan and post-Ramadan body weights was 2.9 kg in obese patients but 0.9 kg in nonobese patients. Moreover, in our study, the BMI of obese patients was significantly reduced, compared to that of nonobese patients. The average reduction in BMI in obese patients was 0.9 kg/m2. Similarly, many studies have reported weight loss during the month of Ramadan fasting.8,9 This can be due to obese subjects trying to eat less at dinner, accepting Ramadan as a chance to lose weight for themselves. In contrast to this, a study from Saudi Arabia reported weight gain during Ramadan, and still others did not find any significant change in body weight.10 Fakhrzadeh et al.11 found that fasting caused a significant reduction in weight and BMI in men and in waist circumference in women.

HOMA-IR In our study, post-Ramadan HOMA-IR values were significantly lower for obese subjects, whereas post-Ramadan HOMA-IR values of nonobese subjects were higher, compared to pre-Ramadan values. Vahdat Shariatpanahi et al. also observed significant decline in HOMA-IR values.14 We could not explain why the post-Ramadan fasting HOMA-IR level in nonobese subjects in the current study was higher. The increase in the HOMA-IR value may be due to an increase in insulin level, but the increase in insulin level was not significant.

Cytokines

We found that the FBG level in obese individuals was significantly reduced, compared to nonobese ones. In several studies, the FBG level was compared, but not between obese and nonobese people. Fakhrzadeh et al.11 found that fasting plasma glucose decreased significantly in both men and women. Khaled et al.12 found significant decreases in fasting serum glucose and glycosylated hemoglobin (HbA1c) in obese women with type 2 diabetes mellitus.

In our study, IL-2, IL-8, and TNF-a were found to be significantly lower after Ramadan fasting in both groups. A study conducted by Aksungar et al. demonstrated that IL6, CRP, and homocysteine levels were significantly lowered during Ramadan in the fasting subjects of both genders, when compared to basal values. They concluded that prolonged intermittent fasting in a model like Ramadan has some positive effects on the inflammatory status of the body.15 Probably, the fasting state has an effect on those markers, without regarding whether one is obese or not.

Blood pressure

Hematological parameters

The mean SBP and DBP of our patients was significantly lower at post-Ramadan measurements, compared to preRamadan measurements. Fakhrzadeh et al.11 found that neither SBP nor DBP was affected by Ramadan fasting. Saleh et al.13 found significant improvement of SBP and DBP.

In our study, the WBC count was found to be significantly lower after Ramadan fasting in both groups. Saleh et al.13 noted significant improvement in the mean levels of hemoglobin. Our study has some limitations. One of them is that the level of physical activity and amount of food intake were not measured. One can suspect that as a result of limiting food intake, physical activities tend to decrease during the month of Ramadan fasting. The second limitation is the small sample size of our study. More reliable results can be possible if a new study is conducted with a larger sample size. In conclusion, Ramadan fasting has beneficial results on our metabolic and anthropometric measurements, especially insulin resistance and BMI. Ramadan fasting provides an excellent opportunity to investigate the effects of the prolonged reduction of meal frequency on body metabolism,

Fasting blood glucose

Lipids We did not find any significant change in LDL-C, HDL-C, and TC levels, but there was a significant decrease in TG level in both groups after Ramadan fasting. Khaled et al.12 found a significant decrease in HDL-C, whereas TC, TGs, and LDL-C levels were increased significantly in obese women with type 2 diabetes mellitus. Saleh et al.13 stated that there was significant improvement in the mean levels of TC, TG, HDL-C, LDL-C, TC/HDL, LDL/HDL, Lp (a), apolipoprotein A-1 (APA), and apolipoprotein B (APB).

EFFECTS OF RAMADAN FASTING ON OBESE INDIVIDUALS such as insulin sensitivity, lipid profile, and inflammatory markers. 9.

Author Disclosure Statement No competing financial interests exist.

10.

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Address correspondence to: ¨ nalacak, M.D. Murat U Tip Faku¨ltesi Aile Hekimligi Anabilim Dali Eskis¸ ehir Osmangazi Universitesi 26480 Eskis¸ ehir Turkey E-mail: [email protected]

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