1 Introduction
Obesity is a global phenomenon that has reached epidemic proportions, affecting both developed and developing countries (1). The worldwide prevalence of obesity is escalating swiftly, with a substantial surge in the past years (2). Obesity is associated with several metabolic disorders and chronic diseases, including type 2 diabetes mellitus (T2DM), cardiovascular diseases (CVD), and certain types of cancer (3, 4). Adipose tissue plays a crucial role in the progression of obesity and its associated health risks (4). Leptin and adiponectin are adipokines that modulate energy balance, cardiometabolism, and low-grade inflammation (5). Leptin levels are elevated in individuals with obesity and are associated with leptin resistance, which is related to various metabolic diseases (6). Leptin affects body mass by reducing food intake and increasing energy intake (7). It also plays a role in the reproductive processes, angiogenesis, blood pressure, glucose and lipid metabolism, bone formation, and immune responses (8–12). Leptin levels are positively correlated with fat mass, resulting in elevated levels in individuals with obesity (13). On the other hand, adiponectin regulates energy expenditure, stimulates appetite, and its secretion escalates in tandem with enhanced insulin sensitivity (6). Adiponectin, the adipokine most abundantly secreted by adipose tissue (7), exhibits a decline in serum concentrations with obesity and is also associated with an elevated risk of T2DM and CVD (14, 15).
Drug and surgical interventions (e.g., bariatric surgery or intragastric balloon) for obesity, despite demonstrating effectiveness, frequently entail a multitude of adverse effects and the recurrence of body mass (16–18). Consequently, efforts must be directed toward dietary and lifestyle modifications, especially those that are abundant in plant-based diets (PBD), since those consuming PBD lower their risk for obesity, CVD, T2DM, and other health conditions (19, 20). PBD are capable of potentially exerting an influence on the quantities of leptin and adiponectin in the human body (21, 22). As per the investigation conducted by Lederer et al. (23), plasma adiponectin concentrations were noticeably higher in females who transitioned from an omnivorous to PBD when compared to those following a diet rich in meat; nevertheless, this study did not observe any significant alterations in plasma leptin concentrations. Another study conducted by Menzel et al. (24) failed to identify any notable variances in inflammatory markers, including adiponectin, between vegans and individuals who consume both plant-and animal-based foods.
While vegetarian and vegan diets have the potential to influence leptin and adiponectin levels, further research is needed to fully understand the impacts of PBD. This includes exploring the benefits of reducing animal food consumption rather than completely eliminating it. PBD focus on foods primarily from plants; however, they are not the same as vegetarian or vegan diets since PBD may include meat and dairy, although proportionately predominating in plant sources such as fruits, vegetables, nuts, seeds, oils, whole grains, legumes, and beans (25). However, it is widely acknowledged that the Mediterranean diet and other vegetarian diets (e.g., semi-vegetarian, flexitarian, pescatarian, lacto-ovo vegetarian, and vegan) are often classified as PBD (26).
Many investigations have examined the correlation between physical activity and leptin and adiponectin levels. A narrative review reported that physical activity (only daily physical activity was measured but not any specific physical exercises) elevated adiponectin and decreased leptin levels while simultaneously lowering body mass index (BMI) and body fat percentage (BFP) (27). Physical activity, either on its own or in conjunction with changes in diet or lifestyle, can reduce the levels of leptin in individuals with prediabetes (19) and obesity (28). In a meta-analysis of seven studies by Jadhav et al. (29), physical activity promotion, with or without dietary or lifestyle modification, reduced leptin levels but had no remarkable effects on adiponectin levels in individuals with prediabetes. Seemingly, there is a weak to moderate relationship between aerobic exercise with increased adiponectin levels and decreased leptin levels (30), but it cannot be neglected and ought to be further examined in conjunction with diet, mainly PBD as a cost-effective, low-risk intervention that may improve obesity and cardiometabolic parameters (31, 32). In terms of different forms of physical activity, it was shown that only aerobic exercise but not other forms led to a rise in adiponectin levels and a decrease in leptin levels. To summarize, engaging in physical activity, particularly aerobic exercise, results in increased adiponectin levels and decreased leptin levels in individuals with prediabetes and diabetes (30).
The combination of both exercise training and PBD would be anticipated to produce an additive effect, which may lead to improved health outcomes after the intervention (33–35). The previous study suggests that a combination of exercise training with the Mediterranean diet is more effective than a normal diet for reducing leptin in overweight/obese adults with metabolic syndrome (36). Nevertheless, these results are not consistently reliable. For example, one study did not suggest further increases in adiponectin with exercise training in combination with Mediterranean diet as compared with non-vegetarian diets (37). However, the combined impact of exercise training combined with PBD has not been elucidated in previous meta-analyses. Therefore, the aim of this study was to determine the impact of exercise training combined with PBD on leptin and adiponectin in adults with or without chronic diseases using a systematic review and meta-analysis method.
2 Methods
2.1 Study registration
The current systematic review and meta-analysis was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines (38) and the Cochrane Handbook of Systematic Reviews of Interventions. The systematic review and meta-analysis was registered prospectively with the International Prospective Register of Systematic Reviews (PROSPERO) under the registration number: CRD42023457202.
2.2 Search strategy
PubMed, Scopus, and Web of Science were the primary databases searched to recognize original research articles, published up until May 2024, using a combination of exercise training and PBD terms and the outcomes (leptin and adiponectin). In addition, reference lists of all included studies and previous relevant meta-analyses (39, 40) were searched to detect records not found during the initial electronic search. The search was limited to articles written in the English language and human studies. There was no limit on publication dates. Studies were limited only based on the age of the participants. Adults were included in the present study. Studies performing PBD combined with exercise training interventions were searched by using the following keywords: “vegetarian diet,” “diet,” “Mediterranean diet,” “vegetarian diet,” “plant-based diet,” “paleolithic diet,” “dietary pattern,” “DASH,” “vegan diet,” “lacto-ovo-vegetarian diet,” and “exercise,” “training,” “exercise training,” “physical activity,” and “adipokine,” “adipocytokine,” “adiponectin,” “leptin.” The search strategy for each database is reported in Supplementary Table S1.
2.3 Eligibility criteria
Studies were eligible for inclusion if they met the following PICO (population, intervention, comparison, and outcome) criteria: (1) For population, adults with or without chronic diseases. (2) For the intervention, studies with exercise training combined with PBD were included. (3) For comparison, the pre- and post-test comparisons for the combined effects of exercise training combined with PBD were required. (4) For outcomes, studies that reported leptin and adiponectin measured using a fully validated method were included.
2.4 Study selection
The study selection process is shown in Figure 1. Following the removal of duplicate studies, titles and abstracts of articles were independently assessed, and then the full texts of potentially eligible studies were reviewed by two reviewers to determine eligibility. Any disagreements were resolved through discussion with another author.
Studies that met the following criteria were included in this systematic review and meta-analysis: (1) randomized controlled trials (RCTs), prospective cohort studies, non-randomized controlled trials (non-RCTs); (2) the types of diets included vegetarian, lacto-ovo vegetarian, lacto-vegetarian, ovo-vegetarian diets, Mediterranean diets, Apulian diet (aphypoD); (3) exercise training types were not limited; (4) studies that examined the effect of exercise training combined with PBD on serum or plasma leptin and adiponectin; and (5) studies that presented outcome data of interest as the mean and standard deviations (SD), mean and standard error of the mean (SEM), or quartile and 95% confidence interval (CI) in the intervention group. The exclusion criteria were as follows: (1) vegetarian participants; (2) other interventions along with exercise training and diet have been applied; (3) studies that were animal studies, narrative reviews, commentaries, letters, books, case reports, case studies, pilot studies, and conferences; and (4) studies that were not published in English language.
2.5 Data extraction
Data extraction was completed independently by 2 researchers, and disagreements were resolved through discussion with a third review author. The following study characteristics were extracted: (A) participant information, including age, biological sex, BMI, health status, and sample size; (B) study design; and (C) exercise training characteristics (type, duration, and frequency); (D) diet characteristics and duration of intervention; and I outcome analysis. For each outcome (leptin, and adiponectin), pre-and post-intervention (mean and SD), or mean differences and associated standard deviations of the experimental group were entered into the meta-analyses to generate forest plots. If the means and standard deviations (SDs) were not reported, the SDs were calculated from standard errors of means (SEM), medians and interquartile ranges (IQRs), or means and IQRs (41–43).
2.6 Quality assessment
The risk of bias was evaluated using the Physiotherapy Evidence Database (PEDro) scale. Two items were omitted from the initial 11-item scale due to factors such as similarity of groups at baseline, absence of blinding for participants and intervention providers, and the inability to obscure the allocated dietary conditions during the studies for both participants and intervention providers. The scale used for the current study consisted of nine items: (1) specified eligibility criteria, (2) randomized participant allocation, (3) concealed allocation, (4) blinding of all assessors, (5) evaluated outcomes in 85% of participants, (6) intention-to-treat (ITT) analysis, (7) reporting of statistical comparisons between groups, (8) and point measures and measures of variability (Supplementary Table S2).
2.7 Statistical analysis
Meta-analyses were performed using the Comprehensive Meta-analysis (CMA) software (version 2.0, United States) to compute standardized mean differences (SMD) and 95% CIs for outcomes using random-effects models. Effect sizes were calculated to compare the impact of exercise training combined with PBD on leptin and adiponectin in adults. Heterogeneity was evaluated by using the I2 statistic, and significance was set at p p 44). Furthermore, the trim and fill method was used to correct the potential effects of publication bias when visual interpretation of funnel plots demonstrated publication bias.
3 Results
3.1 Included studies
Based on our original search technique, we discovered a combined total of 808 articles in PubMed, 136 articles in Scopus, and 1,465 articles in Web of Science. After excluding duplicate records and evaluating the titles and abstracts, 16 studies were determined to be relevant and necessitated a comprehensive assessment of their complete texts. After conducting a detailed assessment of the full texts, five studies were excluded for the following reasons: did not measure leptin and adiponectin (n = 5) levels. In this systematic review and meta-analysis, a total of nine studies were evaluated, which comprised intervention groups involving the combination of exercise training and PBD. The flow diagram of the systematic literature search is shown in Figure 1.
3.2 Participant characteristics
A combined group of 960 adults with different diseases such as metabolic syndrome, obesity, postmenopausal women, obstructive sleep apnea, T2DM, and coronary artery disease were included, with sample sizes ranging from 37 (45) to 266 (46). The average age ranged from 18 years (34) to 75 years (36), while the BMI ranged from 24.6 kg.m−2 (33) to 40 kg.m−2 (36, 46). A total of nine studies were encompassed in the analysis. Among them, seven studies had both males and females (20, 35–37, 45–47), whereas one study only included males (34) and one study only included females (33). The participants’ health status varied across the studies, including healthy elderly participants (47), metabolic syndrome (34, 46), overweight and obesity (20, 36), postmenopausal women (33), obstructive sleep apnea (37), T2DM (45), and coronary artery disease (35). Table 1 provides a more comprehensive breakdown of the characteristics of the participants.
Table 1. Study, participants, and intervention characteristics.
3.3 Intervention characteristics
A combination of exercise training and PBD methodologies was implemented across the included studies in the analysis. Some studies used plant foods with a low glycemic load, low in saturated fats and alcohol, and rich in antioxidants and fiber (33), PBD including soya foods, nuts, seeds, and healthy oils (47), and others used Mediterranean diet including fruits, vegetables, nuts, whole grains, and olive oil daily (34, 36, 37, 46). Additionally, the length of the interventions varied, ranging from 1 week (20) to 24 months (33–37, 45–47). The studies incorporated various forms of exercise training interventions, including moderate-intensity physical activity, moderate- and high-intensity walking, yoga programs, moderate aerobic exercise on a treadmill, swimming or aerobic ball games, or cycling. In most studies, participants exercised 150 min/week. Detailed information about the intervention characteristics can be found in Table 1.
3.4 Meta-analysis
3.4.1 The effects of PBD combined with exercise training on leptin in adults
Based on five intervention arms, PBD combined with exercise training had significantly lower serum concentrations of leptin [SMD = -0.33 (95% CI: −0.62 to −0.04) and p = 0.025] (Figure 2). The studies included in the analysis demonstrated high heterogeneity (I2 = 92.19%, p = 0.001). The absence of publication bias was supported by the results of funnel plots and Egger’s test (p = 0.90). Given that the result of the funnel plots and Egger’s test was not significant, the trim and fill method was not performed.
Figure 2. Forest plot of the effects of exercise training combined with PBD on serum leptin. Data are reported as SMD (95% confidence limits). SMD, standardized mean differences.
3.4.2 The effects of PBD combined with exercise training on adiponectin in adults
Based on five intervention arms, PBD combined with exercise training had significantly higher serum concentrations of adiponectin [SMD = 0.93 (95% CI: 0.12 to 1.74) and p = 0.024] (Figure 3). The studies included in the analysis demonstrated high heterogeneity (I2 = 96.84%, p = 0.001). The existence of publication bias was supported by the results of funnel plots and Egger’s test (p = 0.003). In addition, the trim and fill results showed that the overall changes were as follows: adiponectin [SMD = 0.93 (95% CI: 0.12 to 1.74)]. The results of adiponectin did not change [SMD = 0.93 (95% CI: 0.12 to 1.74)]. Since no bias is present in these simulations all “missing” studies detected are because of chance funnel plot asymmetry.
Figure 3. Forest plot of the effects of exercise training combined with PBD on serum adiponectin. Data are reported as SMD (95% confidence limits). SMD, standardized mean differences.
3.5 Quality assessment
The PEDro tool was used to assess the methodological quality of each individual study, and their scores varied between 3 and 9 out of a possible maximum of 9 points. One study had a score of 9 (37), one study had a score of 8 (33), two studies had scores of 6 (36, 45), four studies had 5 (20, 34, 35, 46), and one study had a score of 3 (47). Most of the PEDro scores were lowered due to three items (concealed allocation, blinding of all assessors, and intention-to-treat analysis). The details of the quality analysis are shown in Supplementary Table S2.
4 Discussion
The aim of this meta-analysis was to investigate the effect of PBD combined with exercise training on leptin and adiponectin levels in adults with or without chronic diseases. The main findings of the study showed that exercise training combined with PBD caused a significant decrease in leptin while a significant increase in the levels of adiponectin in adults. Many studies support these findings (20, 33, 35, 36, 46). Our findings have important implications for understanding the effects of lifestyle modification on leptin regulation and obesity. Leptin is a hormone secreted by adipose tissue and acts centrally in the hypothalamus to regulate energy balance and appetite (48). Higher levels of leptin indicate that the hypothalamus has sufficient fat stores to suppress appetite and increase energy expenditure. Individuals with obesity typically have chronically elevated leptin levels, indicating leptin resistance, in which increased leptin signaling does not translate into appropriate appetite suppressant effects (49). The reduction in leptin observed with dietary and exercise training interventions may contribute to sensitizing the brain to the effects of leptin and better body mass control.
Several mechanisms may underlie the leptin-lowering effects of exercise training. For instance, exercise training has been shown to increase catecholamines such as epinephrine and norepinephrine, which inhibit the production and secretion of leptin in adipose tissue (50). Exercise-induced activation of the sympathetic nervous system can also directly inhibit transcription (51). In addition, the anti-inflammatory effects of exercise training may reduce leptin production, as inflammatory cytokines stimulate leptin secretion (52).
PBD are lower in fat and higher in fiber than omnivorous diets. Inadequate dietary fat consumption significantly contributes to the reduction of circulating leptin, given that acute increases in adipose triglycerides and plasma fatty acids modulate leptin secretion (53). Fiber has also been shown to bind leptin in the small intestine and inhibit its absorption. Additionally, lower amounts of protein in PBD may affect leptin levels, as protein strongly stimulates leptin secretion (22, 54).
The synergistic effect of physical activity and PBD on leptin reduction may be explained by the reduction of fat cell size and total body fat mass (39). Exercise training and negative energy balance activate triglycerides stored in fat cells and reduce fat diameter. The mass of leptin-producing adipose tissue also decreases with body mass loss caused by diet and exercise training. These morphological changes in fat probably underlie the concomitant decrease in plasma leptin levels (55).
These findings have clinical implications for the treatment of obesity. Increased leptin levels are associated with an increased risk of metabolic diseases, cardiovascular events, and some cancers (56). The leptin-lowering effects of aerobic exercise and PBD demonstrated in this meta-analysis may contribute to the reduction in morbidity and mortality observed with these lifestyle changes. For adults with obesity, combining regular aerobic exercise with a Mediterranean diet may be an effective strategy not only for body mass loss but also for improving leptin sensitivity and metabolic health (46).
The results of the current meta-analyses also showed that a combination of PBD with exercise training led to remarkable increases in adiponectin levels in adults. Other studies also support these findings (33, 34, 37, 45, 47). Several mechanisms may contribute to this upregulation of adiponectin by exercise training and PBD. First, exercise training is a potent stimulus for increased adiponectin production and release from adipose tissue. Skeletal muscle contractions during aerobic exercise, such as walking, running, or cycling, stimulate the release of adiponectin into the circulation (57). This may be mediated by the activation of p38 mitogen-activated protein kinase (MAPK) signaling in adipocytes in response to muscle contraction (58). In addition, exercise training reduces inflammation within visceral fat, which may reduce transcriptional and translational repression of adiponectin (59).
Second, PBD are rich in nutrients and bioactive compounds that have been shown to increase adiponectin levels. Specifically, high fiber intake from whole grains, fruits, vegetables, and legumes regulates adiponectin by increasing insulin sensitivity and suppressing inflammatory signals (60). PBD also consist of adequate vitamin C, magnesium, and omega-3 fatty acids from plant sources, all of which are associated with increased adiponectin production (22). Eliminating meat in Mediterranean diets may help by removing pro-inflammatory factors and improving oxidative balance (46).
Together, these synergistic mechanisms induced by aerobic exercise and PBD significantly increase adiponectin levels. The large effect size shown in this meta-analysis is clinically significant, as higher circulating adiponectin is independently associated with a variety of health benefits. Prospective studies show that increased adiponectin reduces the risk of obesity, T2DM, CVD, and some cancers (61). Adiponectin exerts these protective effects through its insulin-sensitizing, anti-inflammatory, and anti-atherogenic properties (62).
Given the increasing prevalence of hypoadiponectinemia in many populations, our findings have important implications. Adiponectin levels have declined significantly over the past few decades, likely due to increased levels of physical inactivity and unhealthy diets high in saturated fat and processed foods (63). Low adiponectin is now thought to be an independent risk factor for insulin resistance, metabolic syndrome, and CVD (64). Therefore, lifestyle modification aimed at increasing adiponectin may provide a powerful therapeutic strategy for the prevention and management of several interrelated chronic diseases.
In summary, the present meta-analysis study showed that a combination of exercise training and PBD decreased circulating leptin levels while increasing adiponectin. The decrease in leptin and increase in adiponectin may be attributed to the decrease in fat mass, as well as the direct effect of exercise training and diet composition on leptin production and secretion. Increasing chronic adiponectin and leptin levels through lifestyle modification may improve leptin sensitivity and obesity-related diseases. Further research is needed to identify long-term clinical effects and determine definitive strategies.
Overall, findings are different regarding the effect of PBD and physical activity on leptin and adiponectin levels. One study showed that PBD had no effect on leptin and adiponectin levels (21), while the other study showed that a short-term intervention with a vegetarian diet resulted in improved plasma concentrations of adiponectin and leptin (23). Certain dietary components that are lower in PBD diets, such as energy intake, saturated fat, heme iron, and red and processed meat, may influence the risk of metabolic syndrome. In addition, PBD contain more fruits, vegetables, and fiber, which protect against metabolic syndrome. Additionally, intensive lifestyle changes, including PBD diet, have been associated with a reduced risk of metabolic syndrome (65).
This meta-analysis has several strengths that lend credence to the results. To the best of our knowledge, the current study is the most comprehensive meta-analysis addressing the effects of PBD combined with exercise training on leptin and adiponectin levels in adults with or without chronic diseases. We minimized the potential for bias in the review process by executing a comprehensive search of the literature and also conducting a systematic review and reporting the meta-analytic results according to the PRISMA guidelines. Nevertheless, some potential limitations should be considered when interpreting these findings. First, diet and exercise programs varied somewhat across trials, which may introduce heterogeneity. Additional standardized intervention studies in different populations could further substantiate the effects on adiponectin. Also, some studies were conducted on healthy people and some on adults with overweight and obesity, which may distort the homogeneity of the results to some extent. One of the reasons for the high heterogeneity can be attributed to the different health characteristics of participants, such as menopause, metabolic syndrome, obstructive sleep apnea, obesity, or coronary artery disease, and the duration of the interventions. Conducting meta-regressions could potentially offer more robust findings in this case. However, the limited number of studies that provided data on BFP and BMI precluded us from conducting meta-regression or subgroup analyses to examine the relationship between leptin and adiponectin with BFP or BMI. Also, due to the small number of studies, it was not possible to perform subgroup analysis based on the type, duration, and intensity of exercise.
5 Conclusion
The findings of the present systematic review and meta-analysis show the important role of PBD combined with exercise training in improving leptin and adiponectin. Exercise training combined with PBD are suggested as non-invasive interventions for reducing leptin and increasing adiponectin levels to control body mass and other disorders related to obesity in adults with or without chronic diseases.
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.
Author contributions
FK: Conceptualization, Data curation, Investigation, Methodology, Project administration, Software, Supervision, Writing – original draft, Writing – review & editing. RF: Conceptualization, Data curation, Investigation, Writing – original draft. RB: Writing – review & editing, Writing – original draft. HS: Writing – review & editing. FD: Funding acquisition, Writing – review & editing.
Funding
The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.
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.
Supplementary material
The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fnut.2024.1465378/full#supplementary-material
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