Skip to main content

SYSTEMATIC REVIEW article

Front. Nutr., 24 June 2022
Sec. Clinical Nutrition
https://doi.org/10.3389/fnut.2022.924097

Role of Honey in Obesity Management: A Systematic Review

  • Department of Physiology, Faculty of Medicine, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia

Obesity is a metabolic disorder that has become critically prevalent throughout the world. Obesity has been linked to other chronic diseases such as diabetes mellitus, cardiovascular diseases and cancer. Natural products such as honey have been investigated for their potential effect on obesity. Hence, this study systematically reviewed the recent literature concerning the effects of honey on obesity in obese animal models and in people with obesity. The Ovid MEDLINE, PubMed, Scopus, Web of Science and Google Scholar electronic databases were searched for relevant articles. A total of 130 relevant articles were obtained from the initial search. Following a thorough screening, nine articles were selected for data extraction, including six animal studies and three clinical trials. In most of the animal studies, honey demonstrated an anti-obesity effect by reducing body weight, body fat composition and adipocyte size, among others. However, supplementation of honey in clinical trials showed conflicting results. Even though honey supplementation did not demonstrate any weight-reducing effect in some of the clinical trials, none of the trials showed that honey increases body weight. However, the results should be interpreted with caution as most of the studies involved animal models and there is a limited number of high quality, randomized, controlled clinical trials.

Systematic Review Registration: https://inplasy.com/inplasy-2022-6-0038/ PROSPERO, identifier 10.37766/inplasy2022.6.0038.

Introduction

Obesity and being overweight are pathological conditions characterized by excessive body mass index (BMI) and/or fat mass (1). Overweight is defined as a BMI greater than or equal to 25 kg/m2, whereas obesity is defined as a BMI greater than or equal to 30 kg/m2 (2). Currently, obesity has reached epidemic proportions worldwide, and the prevalence of obesity is expected to worsen in both developed and developing countries following the changes in dietary patterns and physical activity (3). According to the World Health Organization global status report on non-communicable diseases 2014, 39% of adults are overweight, whereas 13% of people are obese. The percentage of people who are overweight or obese is expected to further increase by 2025 (4).

Obesity is a multifactorial condition with a complicated interplay of genetics and environmental components (1). Convenience and “junk” foods are widely available nowadays and these foods are often highly processed, lack in nutrients, and high in sugar and fat content, all of which can contribute to obesity (5). Factors that contribute to obesity are not only limited to increased calorie intake or decreased physical exercise, but also related to psychological distress and body weight dissatisfaction (6). Additionally, economic progress, increased modernity, urbanization, and globalization have all contributed to the current era's rise in obesity (1).

Obesity results in many pathophysiological complications such as dyslipidemia, hypertension, cardiovascular diseases, diabetes mellitus, and metabolic syndrome. It has also been associated with the development of certain cancers (7). Oxidative stress (8), inflammation (9), and hypoxia (10) are the underlying mechanisms that contribute to obesity-related complications. The main approach to manage obesity is through dietary modification and exercise. Additionally, obesity is managed using pharmacotherapy such as orlistat and bariatric surgery (11). However, both pharmacotherapy and surgical intervention carry certain risks and adverse effects to the patients. Hence, more studies are being conducted to investigate the role of natural products such as honey for managing obesity with minimal side effects (12).

Honey is a natural sweetener that has been regularly used to improve the taste and wholesomeness of food (13). It is a naturally occurring mixture of simple and complex sugars, vitamins, minerals, acids, and enzymes (14). There are about 300 different types of floral honey available globally. The floral source is used to classify different varieties of honey. Among the most known popular varieties of honey include acacia honey, rapeseed honey, buckwheat honey, citrus honey, and multiflora honey (15). Other than that, honey can be classified as raw or processed. Raw honey is more natural and purer than processed honey. Processed honey is heated and bottled in a factory, causing it to lose vitamins, minerals, and other key ingredients (16).

Honey's color, flavor, mineral, and vitamin content are influenced by the flower from which the bees collect the nectar (17). Environmental factors such as flower origin and age, pollen type, climatic factors, and production parameters could influence the quality of honey. Processing methods and storage conditions such as temperature and humidity also impact honey quality (18). Phenolic chemicals are the most common phytochemical substances found in honey (19). Other phytochemical components found in honey include flavonoids, ascorbic acid, catalase, peroxidase, and carotenoids. These components are primarily responsible for honey's antioxidative effect (20). Honey's phytochemical content is also affected by its floral and geographical origins, as well as its processing, handling, and storage (21). The characteristics and phytochemical content of honey are most affected by plant pollen and weather conditions (19).

Honey provides various nutritional benefits such as anti-inflammatory (22), anti-hypertensive, and cardioprotective properties (23, 24), as well as antioxidative effects (2527). It also possesses antibacterial (28), antifungal (29), antiviral (30), and antitumor (31) activities. Honey has also demonstrated the anti-obesity effects in various studies (1, 3235). It is postulated that the active components in honey, such as phenol and flavonoid influence fat metabolism by enhancing lipolysis and preventing lipogenesis (36). Hence, this study was conducted to systematically review the relevant studies on the effect of honey on obesity in obese animal models and in people with obesity. This review may provide scientific backup for honey consumption to control body weight.

Methods

Search Strategy

The relevant studies were obtained from five online databases, namely, PubMed, Scopus, Ovid MEDLINE, Web of Science and Google Scholar from 1980 until May 2022. The last search was performed on 20th May 2022. The following keywords were used: Honey AND obesity OR overweight OR body weight OR BW OR body mass index OR BMI OR fat mass OR FM OR lean mass OR LM OR waist circumference OR WC OR leptin OR adiponectin OR waist-hip ratio OR WHR. A total of nine relevant articles were finally selected, which include studies by Gohar et al. (1), Rafie et al. (32), Ramli et al. (33), Romero-Silva et al. (34), Samat et al. (35), Mushtaq et al. (36), Farakla et al. (37), Yaghoobi et al. (38) and Erejuwa et al. (39).

Study Inclusion and Exclusion Criteria

Only full-length original research articles published in English were included. Any clinical (randomized controlled trial) and preclinical (in vivo) studies reporting the effect of any type of honey on body weight control in obese animal models or people with overweight or obesity, regardless of the route of administration, dose, and duration of intervention were included. Preclinical studies using non-obese animal models were excluded. As for clinical trials, studies involving subjects with other comorbidities and subjects on pharmacological therapies were excluded. Studies using combined preparation of honey with other therapy such as herbal medicine, review articles, news, case reports, book chapters, conference proceedings, abstract, and editorial letters were also excluded from this review.

Study Selection and Article Screening

The literature search and articles screening were performed according to the population, interventions, compare, outcome and study design (PICOS) framework, as follows:

• Population (P): Subjects with obesity or overweight as well as animal models of obesity, regardless of animal species, were included.

• Intervention (I): Honey as an intervention in the experimental group were included.

• Comparison (C): The comparator groups received either no intervention or were treated with relevant conventional drug.

• Outcome (O): Changes in body weight, BMI, waist circumference, waist-hip ratio, body fat mass and percentage.

• Study design (S): Clinical (randomized controlled trial) and preclinical (in vivo) studies.

The articles retrieved from the databases were independently reviewed by six authors (S.B.P, K.K, S.A.S.S, N.H.A, M.H.M and A.U). Any disagreement was resolved by discussion to reach a consensus. The screening of articles was done in three stages. Firstly, articles that did not meet the selection criteria were rejected only based on their titles. Secondly, studies that were irrelevant to honey and obesity were eliminated by reading the abstracts. Finally, articles that did not meet the inclusion criteria were eliminated after a thorough reading of the full text.

Results

Studies Selected

A total of 130 articles were found in five online databases, including 16 articles from Ovid MEDLINE, 31 articles from PubMed, 30 articles from Scopus, 26 articles from Web of Science and 27 articles from Google Scholar. Subsequently, 51 articles were removed due to duplication. After reviewing the titles and abstracts, 70 papers were excluded. The remaining nine full-length original articles were collected and thoroughly reviewed. In total, nine articles published between 2008 and 2020 met the search criteria and were included in this review. Figure 1 showed the summary of article selection process. The experimental model, honey type and source, active compound, dose and duration of treatment, findings, and conclusion of each study were listed in Table 1.

FIGURE 1
www.frontiersin.org

Figure 1. A summary of the literature search and the steps involved in the study selection according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline. Overall, nine studies met the search criteria.

TABLE 1
www.frontiersin.org

Table 1. Characteristics of the included studies. Altogether, nine articles were used for data extraction, including six animal studies and three clinical trials.

Experimental Models

The studies selected consisted of three clinical trials and six animal studies. The experimental models used in the animal studies were diet-induced obese Wistar rats (1, 33, 34, 39) and Sprague Dawley rats (32, 35). The control rats were fed a normal chow diet, while obesity in rats were induced with a hypercaloric diet (HCD) (34), high-fat diet (HFD) (1, 32, 35, 39), and high-carbohydrate and high-fat diet (HCHFD) (33). Some of the animal studies used orlistat as a positive control (32, 35). For clinical trials, the subjects involved were obese prepubertal girls (37) and obese adults (36, 38). Control groups in the clinical trials were supplemented with marmalade (37) and sucrose (38). The duration of honey supplementation varied among the clinical and animal studies. The animal studies involved a shorter duration of honey supplementation between four and 12 weeks, compared to clinical trials, which had a duration of 4 weeks to 6 months. For the animal studies, the doses of honey used varied between 20 and 3,000 mg/kg/day, while the doses used in clinical trials ranged between 15 and 70 g daily.

Types, Sources and Contents of Honey

Malaysia produces various honey, including flower honey (such as honey harvested from trees like Gelam and Tualang trees) and honeydew honey (such as acacia honey), owing to its tropical climate and wealth of floral sources (40). Three of the animal studies used three different types of honey from Malaysia (32, 33, 35). One of them used Gelam honey from Gelam Forest, Terengganu and acacia honey from a farm in Johor (35), while two other studies used stingless bee honey (SBH) obtained from two different states in Malaysia, namely, Kelantan (32) and Selangor (33). Four other animal studies used wild flowers-forest thyme honey from Greece (37), acacia honey from Karachi, Pakistan (1), Alshifa natural honey from Jeddah, Saudi Arabia (36) and honey from Ebonyi State, Nigeria (39). Meanwhile, in the remaining two animal studies, the type and source of the natural honey used were not stated in the articles (34, 38). The active compounds found in honey are phenols (35, 37) and flavonoids (35). One study conducted gas chromatography-mass spectrometry (GC-MS) analysis of SBH and found various active compounds in SBH such as 4-hydroxyphenyl acetic acid, caffeic acid derivatives, caffeoyl hexoside derivatives, coumaric acid, gluconic acid, kynurenic acid derivatives, pinobanksin, quinic acid, niazimicin, bisosthenon B, (6β,7α,12β,13β)-7-hydroxy-11,16-dioxo-8,14-apianadien-22, 6-olide, aegle marmelos alkaloid C, 7-chloro-6-demethyl cepharadione B, n-acetylglycine and lanosterol (33).

Effects of Honey on Obesity

Most of the animal studies have demonstrated that honey has weight-reducing properties, as evidenced by lower body weight, percentage of body weight gain, and BMI (1, 32, 35, 39). However, in two of the animal studies, honey supplementation did not cause a significant reduction or increment in body weight in the obese rats (33, 34). In terms of body fat, honey supplementation lowered the body fat percentage (33), adiposity index (32, 33, 35, 39), and omental fat mass (33). Microscopically, honey consumption led to a lower adipocyte area and adipocyte parameter (33), reduced number of adipocytes in the visceral fat (32) and smaller adipocyte size in the intra-abdominal and mesenteric fats (32, 34).

Honey consumption also decreased the internal organ weight such as the heart (35), lung (35), and liver (32). In terms of adipokine profile, serum adiponectin increased, while serum leptin and resistin decreased when obese rats were fed with honey (35). Furthermore, obese rats that consumed honey also had an increase in locomotor activity (1), and a higher energy efficiency (35), even though their caloric intake remained the same (1). Gelam honey, acacia honey and SBH were more effective in controlling obesity compared to orlistat (32, 35).

Meanwhile, clinical trials have shown conflicting results with the animal studies (3638). Men and women with overweight and obesity who received honey supplementation had significantly lower BMI compared to the control group who received sucrose. However, there were no significant changes in their body weight, body fat weight and percentage, and waist circumference compared to the control group (38). In another trial involving obese prepubertal girls (37), both control and honey-supplemented groups had significant reductions in their body weight and BMI after six months. Both control and honey-supplemented groups were on strict dietary control and exercise. Nevertheless, the reduction in body weight and BMI in the honey-supplemented group was not significant compared to that in the control group. Additionally, honey did not have any effect on postprandial glucose and insulin levels (37). Honey supplementation also did not cause significant BMI reduction in obese men and women from the four different ethnicities (36). Even though honey supplementation did not cause a significant reduction in the subjects' body weight, there was no evidence showing that honey increased their body weight (3638).

Discussion

This study systematically reviewed current studies related to the effect of honey from various sources on obesity in animal studies and clinical trials involving obese subjects. Most of the obesity induction in animal models was achieved through the consumption of HFD as HFD mimicked the common cause of obesity in humans (41). HFD generates a positive energy balance as it is not only high in calories, but it also reduces energy expenditure (1). A positive energy balance results in increased visceral fat deposition and subsequently, abdominal obesity (42). Wistar rats were used in some studies because they acquired weight more quickly when fed with HFD and represented a polygenic diet-induced obesity model (43). Two studies used 7-week-old (35) and three-month old Sprague Dawley rats (32), respectively, which are the favorable age for studying obesity in animal model (44, 45).

Honey demonstrated various anti-obesity actions in animal studies by reducing body weight, BMI, body fat composition, fat mass, adipocyte area, and adipocyte size. The weight-reducing effect of honey could be explained by several mechanisms. Mono-and disaccharides such as glucose, fructose, maltose, and sucrose make up most of honey's composition. These simple sugars are quickly absorbed and metabolized. About 35–45% of honey is made up of fructose (4648), which delays gastric emptying (49) and therefore, reduces food consumption (50). Honey also produces a laxative effect in vivo (47). The laxative effect leads to the rapid removal of water and waste from the body (51). This effect directly reduces body water content but not fat (51), which indirectly reduces body weight because water makes up majority of body composition. It has also been suggested that honey reduces body weight by promoting lipolysis and preventing lipogenesis (36). Besides, glucose oxidase enzyme catalyzes the formation of hydrogen peroxide from glucose in honey (35). Hydrogen peroxide has insulin-mimetic action that improves the metabolic rate, hence contributing to weight loss with honey consumption (5).

The body's energy homeostasis is shifted to a positive energy balance when energy intake exceeds energy expenditure, which promotes adipose tissue gain and leads to obesity (6, 52, 53). A larger calorie intake should theoretically lead to more weight gain, but this is not the case with honey consumption. Supplementation with Gelam honey in HFD-induced obese rats resulted in a higher total food intake, higher energy efficiency, and lower weight gain (35). The higher energy efficiency with honey intake causes the excess food to be turned into energy rather than for body fat storage, hence causing honey-fed rats to gain less weight despite consuming more food (35). A previous study also showed that locomotor activity positively correlates with energy expenditure and is an important contributor to body weight control (54). Decreased locomotor activity leads to a low energy expenditure in HFD-induced obese rats (1). Interestingly, honey supplementation led to a higher locomotor activity in obese rats that caused a greater energy expenditure and consequently weight loss (1).

Honey also influences body weight by modifying adiposity levels. Adipocyte hypertrophy (increased adipocyte size), adipocyte hyperplasia (increased adipocyte number), or a combination of the two factors may cause the expansion of adipose tissue in obesity (55, 56). Adipocyte hypertrophy is the major contributor of increased fat mass in obesity compared with adipocyte hyperplasia. Adipocyte hyperplasia does not contribute much to fat mass because the newly created cells have limited area for fat storage (57). Honey was shown to reduce adipocyte hypertrophy in HCD-induced obese rats (34). In other studies, SBH reduced the area covered by adipocytes in HCHFD-induced obese rats (35), and decreased adipocyte hyperplasia in the visceral fat of HFD-induced rats (32). However, the exact mechanism by which honey lowers adipocyte hypertrophy and hyperplasia remains unclear (32).

The number and size of adipocytes also affect the adiposity index and relative organ weight that eventually affect the body weight. The adiposity index is a method used to measure the body fat distribution (58). It was calculated by dividing the total weight of epididymal, visceral and retroperitoneal fat with the body weight (32). Adipose tissue is an effective buffer against daily lipid fixation in the systemic circulation. When the buffering ability of adipose tissue is compromised, tissues such as skeletal muscles and liver tissue are exposed to lipid accumulation (59). Acacia honey and Gelam honey reduced the relative weight of the liver, heart, and lungs of HFD-fed rats (32). Furthermore, Gelam honey, acacia honey and SBH reduced the adiposity index of obese rats (32, 35). All these factors contribute to the weight-reducing effect of honey.

Adipokines such as adiponectin, leptin, and resistin are released by adipose tissue and their production is altered in obesity. Leptin is a fat-derived key regulator of appetite and energy expenditure, and its plasma concentration is linked to adiposity (60). Resistin is a pro-inflammatory adipokine that suppresses glucose uptake and insulin sensitivity (61). On the other hand, adiponectin is an anti-inflammatory adipokine that enhances insulin sensitivity (62). Obese rats showed increased levels of resistin and leptin, and reduced levels of adiponectin. Supplementation of obese rats with Gelam honey and acacia honey successfully reduced the levels of leptin and resistin, while the adiponectin level was increased (35). These findings suggest that honey causes a significant adipocyte loss, as evidenced by lower leptin and resistin levels, whereas the increased adiponectin levels reduce the weight gain in rats fed with honey (35).

Previous studies have demonstrated that central obesity triggers low-grade systemic inflammation, as evidenced by elevated inflammatory markers such as C-reactive protein, tumor necrosis factor-α, and interleukin-6 in the plasma of people with central obesity (6365). Systemic oxidative stress and chronic inflammation play a critical role in sustaining obesity (66). Gelam honey and acacia honey contain phenolic acids and flavonoids, which are powerful antioxidative and anti-inflammatory compounds (35). Table 2 summarizes the common phenolics acids and flavonoids found in different types of honey. For example, SBH contains coumaric and caffeic acids as its active components. Both coumaric and caffeic acids have anti-obesity effects (8183).

TABLE 2
www.frontiersin.org

Table 2. Common phenolic acids and flavonoids found in different types of honey.

In 3T3-L1 adipocytes, coumaric acid triggers G1 cell cycle arrest (84), whereas caffeic acid inhibits fatty acid synthesis (85). Additionally, gelam honey, SBH, acacia honey and thyme honey contain the flavonoid quercetin, which is a powerful antioxidant (6769). Antioxidants could scavenge free radicals by inhibiting some enzymes or by chelating trace metals (86). It may provide a viable therapeutic approach to alleviate the excessive reactive oxygen species production, oxidative stress, and adverse effects of obesity. Quercetin reduces oxidative stress associated with obesity by modulating the mitogen-activated protein kinase (MAPK) and adenosine monophosphate-activated protein kinase (AMPK) pathways (87). Quercetin inhibits adipogenesis in 3T3-L1 adipocytes by activating AMPK (88) and attenuates macrophage infiltration and inflammation in the adipose tissue of obese mice by enhancing AMPK and sirtuin-1 expression (89). Clinically, consumption of 150 mg/day of quercetin by overweight and obese men with various apolipoprotein E genotypes successfully decreased their waist circumference (90). In short, the anti-obesity effect of honey is most likely mediated by its phenolic acids and flavonoid contents that possess antioxidative and anti-inflammatory activities.

Even though honey has demonstrated promising anti-obesity effects in animal studies, most clinical trials showed that it has no significant weight-reducing effect. Unlike animal studies, confounding factors that can affect body weight such as diet and physical activities, were not controlled in the clinical trials (36, 38). Besides, the clinical trials only include a small sample size, which are 30 obese prepubertal girls (37), 80 obese adults (36) and 60 overweight and obese adults (38). Additionally, the duration of the clinical trials was short, between 30 days (38) to 4 weeks (36). It has been proven that a well-designed, randomized, controlled clinical trial is the most reliable method to determine the effectiveness of an intervention as it reduces the chance of confounding factors from affecting the results (91). Therefore, to determine the effect of honey on obesity in humans, more high-quality, randomized, controlled clinical trials are needed.

Nevertheless, the prevalence of obesity differs with sex and racial ethnic identity. For instance, in the United States of America, the prevalence of obesity is highest among non-Hispanic Blacks and Hispanics, and lower among Asians and non-Hispanic whites (92). In most countries, obesity is more prevalent in women than men (93). This pattern has been attributed to genetic factor that affect body composition and fat distribution, as well as socioeconomic factors (94, 95). Only one clinical trial evaluated the effect of honey on the BMI of obese men and women from four different ethnic groups in Pakistan: Baloch, Pathan, Hazara and Punjabi. The results showed that honey supplementation did not cause any significant BMI reduction in obese men and women of all four ethnicities (36). However, the participants were not subjected to any dietary control or physical activity regime. Further studies involving different ethnic backgrounds are needed to ascertain the role of different sex and race on the effect of honey in obesity.

Conclusion

Honey exerts anti-obesity effects in animal studies by reducing body weight, BMI, body fat composition, adiposity index, adipocyte hypertrophy and adipocyte hyperplasia. However, most clinical trials show insignificant results due to the small sample size, limited treatment duration and the presence of confounding factors such as diet and physical activity. Therefore, more high quality, randomized, controlled clinical trials are needed to establish the effect of honey in obese humans.

Data Availability Statement

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

Author Contributions

AU, JK, and MM contributed to conception and design. SS, NA, SP, KK, AA, AH, and NS contributed to data acquisition. SS, NA, SP, KK, NS, and AU were involved in analysis and interpretation and drafting the manuscript. AU, JK, AA, AH, and MM revise the manuscript critically for important intellectual content. All authors contributed to the article and approved the submitted version.

Funding

This research was funded by Faculty of Medicine, Universiti Kebangsaan Malaysia (grant code FF-2021-235) under the Special Study Module.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

The authors would like to thank the committee members of the Special Study Module, Faculty of Medicine, Universiti Kebangsaan Malaysia.

References

1. Gohar A, Shakeel M, Atkinson RL, Haleem DJ. Potential mechanisms of improvement in body weight, metabolic profile, and liver metabolism by honey in rats on a high fat diet. PharmaNutrition. (2020) 14:100227. doi: 10.1016/j.phanu.2020.100227

CrossRef Full Text | Google Scholar

2. WHO. (2021). Obesity and overweight. Available online at: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight (accessed May 20, 2022).

Google Scholar

3. Flegal KM, Graubard BI, Williamson DF, Gail M.H. Excess deaths associated with underweight, overweight, and obesity. JAMA. (2005) 293:1861–7. doi: 10.1001/jama.293.15.1861

PubMed Abstract | CrossRef Full Text | Google Scholar

4. World Obesity Federation. World Obesity Day: “All countries significantly off track to meet 2025 WHO targets on Obesity”. (2020). Available online at: https://www.worldobesity.org/news/world-obesity-day-all-countries-significantly-off-track-to-meet-2025-who-targets-on-obesity (accessed December 15, 2021).

Google Scholar

5. Chepulis LM. The effect of honey compared to sucrose, mixed sugars, and a sugar-free diet on weight gain in young rats. J Food Sci. (2007) 72:S224–9. doi: 10.1111/j.1750-3841.2007.00286.x

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Haleem DJ, Mahmood K. Brain serotonin in high-fat diet-induced weight gain, anxiety and spatial memory in rats. Nutr Neurosci. (2021) 24:226–35. doi: 10.1080/1028415X.2019.1619983

PubMed Abstract | CrossRef Full Text | Google Scholar

7. Power C, Pinto Pereira SM, Law C, Ki M. Obesity and risk factors for cardiovascular disease and type 2 diabetes: Investigating the role of physical activity and sedentary behaviour in mid-life in the 1958 British cohort. Atherosclerosis. (2014) 233:363–9. doi: 10.1016/j.atherosclerosis.2014.01.032

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies. Metab Syndr Relat Disord. (2015) 13:423–44. doi: 10.1089/met.2015.0095

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Ellulu MS, Patimah I, Khaza H, Rahmat A, Abed Y, Sci AM. Obesity and inflammation : the linking mechanism and the complications. Arch Med Sci. (2016) 8:51–63. doi: 10.5114/aoms.2016.58928.

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Norouzirad R, González-Muniesa P, Ghasemi A. Hypoxia in obesity and diabetes: potential therapeutic effects of hyperoxia and nitrate. Oxid Med Cell Longev. (2017) 3:267. doi: 10.1155/2017/5350267

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Nwobodo NN. Toxicity and safety concerns in orlistat therapy for obesity: a critical evaluation. Asian J Biomed Pharm Sci. (2015) 5:01–4. doi: 10.15272/ajbps.v5i47.725

CrossRef Full Text | Google Scholar

12. Sharma M, Dwivedi P, Singh Rawat AK, Dwivedi AK. Nutrition nutraceuticals: a proactive approach for healthcare. Nutraceuticals. (2016) 4:79–116. doi: 10.1016/B978-0-12-804305-9.00003-8

CrossRef Full Text | Google Scholar

13. Alvarez-Suarez JM, Tulipani S, Romandini S, Bertoli E, Battino M. Contribution of honey in nutrition and human health: a review. Med J Nutrition Metab. (2010) 3:15–23. doi: 10.1007/s12349-009-0051-6

PubMed Abstract | CrossRef Full Text | Google Scholar

14. Cooper RA, Molan PC, Harding KG. Antibacterial activity of honey against strains of Staphylococcus aureus from infected wounds. J R Soc Med. (1999) 92:283–5. doi: 10.1177/014107689909200604

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Janda K, Jakubczyk K, Wozniak K, Stepień E. The influence of temperature on the antioxidant potential in different types of honey. Postepy hig med dosw (online). (2020) 74:42–8. doi: 10.5604/01.3001.0013.8611

CrossRef Full Text | Google Scholar

16. Dabur Honey. Different Types of Honey & their Benefits/Uses. Available online at: https://www.daburhoney.com/benefits-of-honey/honey-for-health/types-of-honey (accessed December 15, 2021).

Google Scholar

17. Zaghloul A. A., el-Shattawy H.H., Kassem A.A., et al. Honey, a prospective antibiotic: extraction, formulation, and stability. Die Pharmazie. (2001) 56:643-647.

PubMed Abstract | Google Scholar

18. Alwazeer D., Yurt B. (2015). Factors Affecting Honey Composition. In: FHTT: From Hive to Table; 2015 May 21-22; Istanbul, Turki, p:78.

Google Scholar

19. Khalil MI, Alam N, Moniruzzaman M, Sulaiman SA, Gan SH. Phenolic Acid Composition and antioxidant properties of Malaysian honeys. J Food Sci. (2011) 76:921–8. doi: 10.1111/j.1750-3841.2011.02282.x

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Gheldof N, Engeseth NJ. Antioxidant capacity of honeys from various floral sources based on the determination of oxygen radical absorbance capacity and inhibition of in vitro lipoprotein oxidation in human serum samples. J Agric Food Chem. (2002) 50:3050–5. doi: 10.1021/jf0114637

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Al-Mamary M, Al-Meeri A, Al-Habori M. Antioxidant activities and total phenolics of different types of honey. Nutr Res. (2002) 22:1041–7. doi: 10.1016/S0271-5317(02)00406-2

CrossRef Full Text | Google Scholar

22. Kassim M, Achoui M, Mustafa MR, Mohd MA, Yusoff KM. Ellagic acid, phenolic acids, and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Nutr Res. (2010) 30:650–9. doi: 10.1016/j.nutres.2010.08.008

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Rakha MK, Nabil ZI, Hussein AA. Cardioactive and vasoactive effects of natural wild honey against cardiac malperformance induced by hyperadrenergic activity. J Med Food. (2008) 11:91–8. doi: 10.1089/jmf.2006.172

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Erejuwa OO, Nwobodo NN, Akpan JL, Okorie UA, Ezeonu CT, Ezeokpo BC, et al. Nigerian honey ameliorates hyperglycemia and dyslipidemia in alloxan-induced diabetic rats. Nutrients. (2016) 8:30095. doi: 10.3390/nu8030095

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Munstedt K, Bohme M, Hauenschild A, Hrgovic IX, Consumption of rapeseed honey leads to higher serum fructose levels compared with analogue glucose/fructose solutions. Eur J Clin Nutr [Internet]. (2011) 65:77–80. doi: 10.1038/ejcn.2010.186

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Omotayo EO, Gurtu S, Sulaiman SA, Wahab MSA, Sirajudeen KNS, Salleh MSM. Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int J Vitam Nutr Res [Internet]. (2010) 80:74–82. doi: 10.1024/0300-9831/a000008

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Spilioti E, Jaakkola M, Tolonen T, Lipponen M, Virtanen V, Chinou I, et al. Phenolic acid composition, antiatherogenic and anticancer potential of honeys derived from various regions in Greece. PLoS ONE. (2014) 9:1–10. doi: 10.1371/journal.pone.0094860

PubMed Abstract | CrossRef Full Text | Google Scholar

28. Tan HT, Rahman RA, Gan SH, Halim AS, Hassan SA, Sulaiman SA, et al. The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complement Altern Med. (2014).9:34. doi: 10.1186/1472-6882-9-34

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Feás X., Estevinho M.L. Survey of the in vitro antifungal activity of heather (Erica Sp.) Organic honey. J Med Food. (2011) A 14:1284–8. doi: 10.1089/jmf.2010.0211

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Zeina B, Othman O, Al-Assad S. Effect of honey versus thyme on Rubella virus survival in vitro. J Altern Complement Med. (1996) 2:345–8. doi: 10.1089/acm.1996.2.345

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Takeuchi M, Fukuda M, Kobayashi K, Hirono Y, Miyagawa M, Ishida T, et al. (2011). Jungle honey enhances immune function and antitumor activity Evidence-based Complement. Altern Med. (2011) 2:86. doi: 10.1093/ecam/nen086

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Rafie AZM, Syahir A, Ahmad WANW, Mustafa MZ, Mariatulqabtiah AR. Supplementation of stingless bee honey from heterotrigona itama improves antiobesity parameters in high-fat diet induced obese rat model evidence-based complement. Altern Med. (2018) 3:1582. doi: 10.1155/2018/6371582

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Ramli NZ, Chin KY, Zarkasi KA, Ahmad F. The beneficial effects of stingless bee honey from Heterotrigona itama against metabolic changes in rats fed with high-carbohydrate and high-fat diet. Int J Environ Res Public Health. (2019) 16”4987. doi: 10.3390/ijerph16244987

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Romero-Silva S, Angel Martinez RM, Romero-Romero L, Rodriguez O, Gerardo Salas GC., Morel N, et al. Effects of honey against the accumulation of adipose tissue and the increased blood pressure on carbohydrate-induced obesity in rat. Lett Drug Des Discov. (2010). 8:69–75. doi: 10.2174/157018011793663912

CrossRef Full Text | Google Scholar

35. Samat S, Kanyan Enchang F, Nor Hussein F, Wan Ismail WI. 4-Week consumption of malaysian honey reduces excess weight gain and improves obesity-related parameters in high fat diet induced obese rats. Evid based complement. Alternat Med. (2017) 2017:1342150. doi: 10.1155/2017/1342150

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Mushtaq R, Mushtaq R, Khan ZT. Effects of natural honey on lipid profile and Body weight in normal weight and obese adults: a randomized clinical trial. Pak J Zool. (2011) 43:161–9. Available online at: https://www.zsp.com.pk

Google Scholar

37. Farakla I, Koui E, Arditi J, Papageorgiou I, Bartzeliotou A, Papadopoulos G, et al. Effect of honey on glucose and insulin concentrations in obese girls. Eur J Clin Invest. (2019) 49:13042. doi: 10.1111/eci.13042

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Yaghoobi N, Al-Waili N, Ghayour-Mobarhan M, Parizadeh SMR, Abasalti Z, Yaghoobi Z, et al. Natural honey and cardiovascular risk factors; effects on blood glucose, cholesterol, triacylglycerole, CRP, and body weight compared with sucrose. ScientificWorldJournal. (2008) 8:463–9. doi: 10.1100/tsw.2008.64

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Erejuwa O, Ezeokpo B, Hospital FT, Nwobodo N, Nwadike KI. Effect of honey on body weight, body mass index and adiposity in high-fat diet fed wistar rats. EC Pharmacol Toxicol. (2017) 31:3–12. Available online at: https://www.ecronicon.com/ECPT.php

Google Scholar

40. Moniruzzaman M, Sulaiman SA, Azlan SAM, Gan SH. Two-year variations of phenolics, flavonoids and antioxidant contents in acacia honey. Molecules. (2013) 18:14694–710. doi: 10.3390/molecules181214694

PubMed Abstract | CrossRef Full Text | Google Scholar

41. Gadja A,=M. High fat diets for diet-induced obesity models. Res Diets. (2008) 10:8247.

Google Scholar

42. Erejuwa OO, Sulaiman SA, Ab Wahab MS, Sirajudeen KNS, Salleh S, Gurtu S. Honey supplementation in spontaneously hypertensive rats elicits antihypertensive effect via amelioration of renal oxidative stress. Oxid Med Cell Longev. (2012) 2012:7–9. doi: 10.1155/2012/374037

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Marques C, Meireles M, Norberto S, Leite J, Freitas J, Pestana D, et al. High-fat diet-induced obesity rat model: a comparison between wistar and sprague-dawley rat. Adipocyte. (2016) 5:11–21. doi: 10.1080/21623945.2015.1061723

PubMed Abstract | CrossRef Full Text | Google Scholar

44. Erejuwa OO, Sulaiman SA, Wahab MS, Sirajudeen KNS, Salleh MS, Gurtu S. Hepatoprotective effect of tualang honey supplementation in streptozotocin-induced diabetic rats. Int J Appl Res Nat Prod. (2011) 4:37–41. Available online at: http://www.ijarnp.org/index.php/ijarnp

Google Scholar

45. Garba AM. The effects of honey and aloe vera extract on ibuprofen induced liver damage in rats. IOSR J Pharm Biol Sci. (2012) 3:6–10. Available online at: https://www.iosrjournals.org/

Google Scholar

46. Nobigrot T, Chasalow FI, Lifshitz F. Carbohydrate absorption from one serving of fruit juice in young children: age and carbohydrate composition effects. J Am Coll Nutr. (1997) 16:152–8. doi: 10.1080/07315724.1997.10718666

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Qiu PY, Ding HB, Tang YK, Xu RJ. Determination of chemical composition of commercial honey by near-infrared spectroscopy. J Agric Food Chem. (1999) 47:2760–5. doi: 10.1021/jf9811368

PubMed Abstract | CrossRef Full Text | Google Scholar

48. Rumessen JJ. Fructose and related food carbohydrates: Sources, intake, absorption, and clinical implications. Scand J Gastroenterol. (1992) 27:819–28. doi: 10.3109/00365529209000148

PubMed Abstract | CrossRef Full Text | Google Scholar

49. Chepulis L. Healing honey: a natural remedy for better health and wellness. Florida: Universal-Publishers (2008) 15.

PubMed Abstract | Google Scholar

50. Brand Miller JC, Lobbezoo I. Replacing starch with sucrose in a high glycaemic index breakfast cereal lowers glycaemic and insulin responses. Eur J Clin Nutr. (1994) 48:749–52.

PubMed Abstract | Google Scholar

51. Martin M, Schlabach G, Shibinski K. The use of nonprescription weight loss products among female basketball, softball, and volleyball athletes from NCAA division I institutions: Issues and concerns. J Athl Train. (1998) 33:41–4.

PubMed Abstract | Google Scholar

52. Choi MS, Kim YJ, Kwon EY, Ryoo JY, Kim SR, Jung UJ. High-fat diet decreases energy expenditure and expression of genes controlling lipid metabolism, mitochondrial function and skeletal system development in the adipose tissue, along with increased expression of extracellular matrix remodelling- and inflammation-related genes. Br J Nutr. (2015) 113:867–77. doi: 10.1017/S0007114515000100

PubMed Abstract | CrossRef Full Text | Google Scholar

53. Mercer JG, Archer Z.A. Diet-induced obesity in the Sprague-Dawley rat: Dietary manipulations and their effect on hypothalamic neuropeptide energy balance systems. Biochem Soc Trans. (2005) 33:1068–72. doi: 10.1042/BST0331068

PubMed Abstract | CrossRef Full Text | Google Scholar

54. Bjursell M, Gerdin AK, Lelliott CJ, Egecioglu E, Elmgren A, Törnell J, et al. Acutely reduced locomotor activity is a major contributor to Western diet-induced obesity in mice. Am J Physiol - Endocrinol Metab. (2008) 294:251–60. doi: 10.1152/ajpendo.00401.2007

PubMed Abstract | CrossRef Full Text | Google Scholar

55. De Ferranti S, Mozaffarian D. The perfect storm: Obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem. (2008) 54:945–55. doi: 10.1373/clinchem.2007.100156

PubMed Abstract | CrossRef Full Text | Google Scholar

56. Hausman DB, Fine JB, Tagra K, Fleming SS, Martin RJ, DiGirolamo M. Regional fat pad growth and cellularity in obese zucker rats: Modulation by caloric restriction. Obes Res. (2003) 11:674–82. doi: 10.1038/oby.2003.96

PubMed Abstract | CrossRef Full Text | Google Scholar

57. Jo J, Gavrilova O, Pack S, Jou W, Mullen S, Sumner AE, et al. Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput Biol. (2009) 5:324. doi: 10.1371/journal.pcbi.1000324

PubMed Abstract | CrossRef Full Text | Google Scholar

58. Jabłonowska-Lietz B, Wrzosek M, Włodarczyk M, Nowicka G. New indexes of body fat distribution, visceral adiposity index, body adiposity index, waist-to-height ratio, and metabolic disturbances in the obese. Kardiol Pol. (2017) 75:1185–91. doi: 10.5603/KP.a2017.0149

PubMed Abstract | CrossRef Full Text | Google Scholar

59. Frayn K. Adipose tissue as a buffer for daily lipid flux. Diabetologia. (2002) 45:1201–10. doi: 10.1007/s00125-002-0873-y

PubMed Abstract | CrossRef Full Text | Google Scholar

60. Handjieva-Darlenska T, Boyadjieva N. The effect of high-fat diet on plasma ghrelin and leptin levels in rats. J Physiol Biochem. (2009) 65:157–64. doi: 10.1007/BF03179066

PubMed Abstract | CrossRef Full Text | Google Scholar

61. Kageyama H. Resistin. Handbook of Hormones: Comparative Endocrinology for Basic and Clinical Research. 1st ed. Cambridge: Academic Press (2016).

Google Scholar

62. Khoramipour K, Chamari K, Hekmatikar AA, Ziyaiyan A, Taherkhani S, Elguindy NM, et al. Adiponectin: structure, physiological functions, role in diseases, and effects of nutrition. Nutrients. (2021) 13:1–15. doi: 10.3390/nu13041180

PubMed Abstract | CrossRef Full Text | Google Scholar

63. Calder P.C., Ahluwalia N., Brouns F., Buetler T., Clement K., Cunningham K., et al. Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr. (2011) 106(SUPPL. 3). doi: 10.1017/S0007114511005460

PubMed Abstract | CrossRef Full Text | Google Scholar

64. Cook DG, Mendall MA, Whincup PH, Carey IM, Ballam L, Morris JE, et al. C-reactive protein concentration in children: relationship to adiposity and other cardiovascular risk factors. Atherosclerosis. (2000) 149:139–50. doi: 10.1016/S0021-9150(99)00312-3

PubMed Abstract | CrossRef Full Text | Google Scholar

65. Panagiotakos DB, Pitsavos C, Yannakoulia M, Chrysohoou C, Stefanadis C. The implication of obesity and central fat on markers of chronic inflammation: the ATTICA study. Atherosclerosis. (2005) 183:308–15. doi: 10.1016/j.atherosclerosis.2005.03.010

PubMed Abstract | CrossRef Full Text | Google Scholar

66. Tun S, Spainhower CJ, Cottrill CL, Lakhani HV, Pillai SS, Dilip A, et al. Therapeutic efficacy of antioxidants in ameliorating obesity phenotype and associated comorbidities. Front Pharmacol. (2020). 11(August):1–20. doi: 10.3389/fphar.2020.01234

PubMed Abstract | CrossRef Full Text | Google Scholar

67. Putri Shuhaili S., Haszianaliza H., Muhammad Fairuz A., Zar Chi T. (2016). Gelam Honey : A Review of Its Antioxidant, Anti- inflammatory, Anticancer and Wound Healing Aspects. 11(2):105-116. doi: 10.17576/MH.2016.1102.01

CrossRef Full Text | Google Scholar

68. Zulkhairi Amin FA, Sabri S, Mohammad SM, Ismail M, Chan KW, Ismail N, et al. Therapeutic properties of stingless bee honey in comparison with european bee honey. Adv Pharmacol Sci. (2018) 2018:6179596. doi: 10.1155/2018/6179596

PubMed Abstract | CrossRef Full Text | Google Scholar

69. Cianciosi D, Forbes-Hernández TY, Afrin S, Gasparrini M, Reboredo-Rodriguez P, Manna PP, et al. Phenolic compounds in honey and their associated health benefits: a review. Molecules (2018) 23:2322. doi: 10.3390/molecules23092322

PubMed Abstract | CrossRef Full Text | Google Scholar

70. Sobral F, Calhelha RC, Barros L, Dueñas M, Tomás A, Santos-Buelga C, et al. Flavonoid Composition and Antitumor Activity of Bee Bread Collected in Northeast Portugal. Molecules. (2017) 22:248. doi: 10.3390/molecules22020248

PubMed Abstract | CrossRef Full Text | Google Scholar

71. Ismail NI, Rafiq M, Kadir A, Zulkifli RM. Isolation and identification of potential antineoplastic bioactive phenolic compounds in Malaysian honeys. J App Pharmaceut Sci. (2015). 5(10):59–66. doi: 10.7324/JAPS.2015.501011

CrossRef Full Text | Google Scholar

72. Wang J., Fang X., Ge L., Cao F., Zhao L., Wang Z., et al. (2018). Antitumor, antioxidant and anti-inflammatory activities of kaempferol and its corresponding glycosides and the enzymatic preparation of kaempferol. PLoS ONE. (2018) 5:1–12. doi: 10.1371/journal.pone.0197563

PubMed Abstract | CrossRef Full Text | Google Scholar

73. Sharifi-Rad J, Quispe C, Imran M, Rauf A, Nadeem M, Gondal TA, et al. Genistein : an integrative overview of its mode of action, pharmacological properties, and health benefits. Oxidative Med Cellular Long. (2021) 2021:813. doi: 10.1155/2021/32681362021

PubMed Abstract | CrossRef Full Text | Google Scholar

74. Rahman MM, Gan SH, Khalil I. Neurological Effects of Honey : Current and Future Prospects. Evidence-Based Complementary and Alternative Medicine. (2014) 2014. doi: 10.1155/2014/958721

PubMed Abstract | CrossRef Full Text | Google Scholar

75. Talebi M, Talebi M, Farkhondeh T, Kopustinskiene DM, Simal-Gandara J, Bernatoniene J, et al. An updated review on the versatile role of chrysin in neurological diseases: Chemistry, pharmacology, and drug delivery approaches. Biomed Pharmacother. (2021) 141:111906. doi: 10.1016/j.biopha.2021.111906

PubMed Abstract | CrossRef Full Text | Google Scholar

76. Yoon CH, Chung SJ, Lee SW, Park YB, Lee SK, Park MC. Gallic acid, a natural polyphenolic acid, induces apoptosis and inhibits proinflammatory gene expressions in rheumatoid arthritis fibroblast-like synoviocytes. Jt Bone Spine. (2013) 80:274–9. doi: 10.1016/j.jbspin.2012.08.010

PubMed Abstract | CrossRef Full Text | Google Scholar

77. Espíndola KMM, Ferreira RG, Narvaez LEM, Silva Rosario ACR, da Silva AHM, Silva AGB, et al. Chemical and pharmacological aspects of caffeic acid and its activity in hepatocarcinoma. Front Oncol. (2019) 9. doi: 10.3389/fonc.2019.00541

PubMed Abstract | CrossRef Full Text | Google Scholar

78. Tajik N, Tajik M, Mack I, Enck P. The potential effects of chlorogenic acid, the main phenolic components in coffee, on health: a comprehensive review of the literature. Eur J Nutr. (2017) 56:2215–44. doi: 10.1007/s00394-017-1379-1

PubMed Abstract | CrossRef Full Text | Google Scholar

79. Ilavenil S, Kim DH, Srigopalram S., Arasu MV, Lee KD, Lee JC, et al. Potential application of p-coumaric acid on differentiation of C2C12 skeletal muscle and 3T3-L1 preadipocytes—an in vitro and in silico approach. Molecules. (2016) 21:997. doi: 10.3390/molecules21080997

PubMed Abstract | CrossRef Full Text | Google Scholar

80. Zduńska K, Dana A, Kolodziejczak A, Rotsztejn H. Antioxidant properties of ferulic acid and its possible application. Skin Pharmacol Physiol. (2018) 31:332–6. doi: 10.1159/000491755

PubMed Abstract | CrossRef Full Text | Google Scholar

81. Jayarathne S., Koboziev I., Park O.H., Oldewage-Theron W., Shen C.L, Moustaid-Moussa N. (2017). Anti-Inflammatory and Anti-Obesity Properties of Food Bioactive Components: Effects on Adipose Tissue. Prev Nutr Food Sci. 22(4):251–62. doi: 10.3746/pnf.2017.22.4.251.

PubMed Abstract | CrossRef Full Text | Google Scholar

82. Jayarathne S., Stull A.J., Miranda A., Scoggin S., Claycombe-Larson K., Kim. J.H., et al. (2018). Tart cherry reduces inflammation in adipose tissue of zucker fatty rats and cultured 3T3-L1 adipocytes. Nutrients. 10(11). doi: 10.3390/nu10111576

PubMed Abstract | CrossRef Full Text | Google Scholar

83. Zhao WH, Zhao CY, Gao LF, Feng FF, Gao W, Chen ZL, et al. The novel inhibitory effect of pangdahai on fatty acid synthase. IUBMB Life. (2008) 60:185–94. doi: 10.1002/iub.28

PubMed Abstract | CrossRef Full Text | Google Scholar

84. Hsu CL, Huang SL, Yen GC. Inhibitory effect of phenolic acids on the proliferation of 3T3-L1 preadipocytes in relation to their antioxidant activity. J Agric Food Chem. (2006) 54:4191–7. doi: 10.1021/jf0609882

PubMed Abstract | CrossRef Full Text | Google Scholar

85. Cho A.S., Jeon S.M., Kim M.J., Yeo J., Seo K. Il., Choi M.S., et al. (2010). Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food Chem Toxicol. 48(3):937–43. doi: 10.1016/j.fct.2010.01.003

PubMed Abstract | CrossRef Full Text | Google Scholar

86. Dai J, Mumper RJ. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules. (2010) 15:7313–52. doi: 10.3390/molecules15107313

PubMed Abstract | CrossRef Full Text | Google Scholar

87. Nabavi SF, Russo GL, Daglia M, Nabavi SM. Role of quercetin as an alternative for obesity treatment: you are what you eat! Food Chem. (2015) 179:305–10. doi: 10.1016/j.foodchem.2015.02.006

PubMed Abstract | CrossRef Full Text | Google Scholar

88. Ahn J, Lee H, Kim S, Park J, Ha T. The anti-obesity effect of quercetin is mediated by the AMPK and MAPK signaling pathways. Biochem Biophys Res Commun 2008. (2008) 373:545–9. doi: 10.1016/j.bbrc.2008.06.077

PubMed Abstract | CrossRef Full Text | Google Scholar

89. Dong J, Zhang X, Zhang L, Bian HX, Xu N, Bao B, et al. Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including AMPKα1/SIRT1. J Lipid Res. (2014) 55:363–74. doi: 10.1194/jlr.M038786

PubMed Abstract | CrossRef Full Text | Google Scholar

90. Pfeuffer M, Auinger A, Bley U, Kraus-Stojanowic I, Laue C, Winkler P, et al. Effect of quercetin on traits of the metabolic syndrome, endothelial function and inflammation in men with different APOE isoforms. Nutr Metab Cardiovasc Dis. (2013) 23:403–9. doi: 10.1016/j.numecd.2011.08.010

PubMed Abstract | CrossRef Full Text | Google Scholar

91. Akobeng AK. Principles of evidence based medicine. Arch Dis Child. (2005) 90:837–40. doi: 10.1136/adc.2005.071761

PubMed Abstract | CrossRef Full Text | Google Scholar

92. Liu B, Du Y, Wu Y, Snetselaar LG, Wallace RB, Bao W. Trends in obesity and adiposity measures by race or ethnicity among adults in the United States 2011-18: population based study. BMJ. (2021) 2021:372. doi: 10.1136/bmj.n365

PubMed Abstract | CrossRef Full Text | Google Scholar

93. Cooper AJ, Gupta SR, Moustafa AF, Chao AM. Sex/Gender Differences in Obesity Prevalence, Comorbidities, and Treatment. Curr Obes Rep. (2021) 10:458–66. doi: 10.1007/s13679-021-00453-x

PubMed Abstract | CrossRef Full Text | Google Scholar

94. Seamans MJ, Robinson WR, Thorpe RJJ, Cole SR, LaVeist TA. Exploring racial differences in the obesity gender gap. Ann Epidemiol. (2015) 25:420–5. doi: 10.1016/j.annepidem.2015.03.010

PubMed Abstract | CrossRef Full Text | Google Scholar

95. Wells JCK, Marphatia AA, Cole TJ, McCoy D. Associations of economic and gender inequality with global obesity prevalence: understanding the female excess. Soc Sci Med. (2012) 75:482–90. doi: 10.1016/j.socscimed.2012.03.029

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: adipose tissue, body mass index, body weight, honey, obesity

Citation: Ugusman A, Shahrin SAS, Azizan NH, Pillai SB, Krishnan K, Salamt N, Aminuddin A, Hamid AA, Kumar J and Mokhtar MH (2022) Role of Honey in Obesity Management: A Systematic Review. Front. Nutr. 9:924097. doi: 10.3389/fnut.2022.924097

Received: 20 April 2022; Accepted: 02 June 2022;
Published: 24 June 2022.

Edited by:

MoezAlIslam Ezzat Faris, University of Sharjah, United Arab Emirates

Reviewed by:

Aisha Musaazi Sebunya Nakitto, Makerere University, Uganda
Shadi Gholami, Harvard Medical School, United States

Copyright © 2022 Ugusman, Shahrin, Azizan, Pillai, Krishnan, Salamt, Aminuddin, Hamid, Kumar and Mokhtar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Azizah Ugusman, dr.azizah@ppukm.ukm.edu.my; Mohd Helmy Mokhtar, helmy@ukm.edu.my

Download