Thinned peach polyphenols alleviate obesity in high fat mice by affecting gut microbiota

https://doi.org/10.1016/j.foodres.2022.111255Get rights and content

Highlights

Abstract

The aim of this study was to explore the anti-obesity activity of thinned peach polyphenols (TPP) and their effects on gut microbiota. An obese mouse model was established using a high-fat diet, and high-throughput sequencing was used to analyze changes in gut microbiota in mice fed with TPP. The results showed that dietary TPP reduced body weight, promoted appetite, reduced liver injury, and reduced levels of TC, TG, LDL-C, ASL and ALT while increasing HDL-C. TPP also enhanced the richness and diversity of gut microbiota in later stages of feeding. Composition and correlation analysis indicated that TPP increased probiotics (such as Alistipes, Akkermansia, Klebsiella, Bacteroides) which negatively correlate with obesity. TPP also reduced the numbers of harmful bacteria (including Helicobacter, Anaeroplasma), which positively correlate with obesity. Probiotics and harmful bacteria cluster independently and the two groups affect each other negatively. These results suggest that TPP reduced obesity by affecting the composition of the gut microbiota in mice. TPP can therefore be used as an ingredient in food to prevent the development of obesity.

Introduction

Obesity is an increasing threat to public health throughout the world. According to the World Health Organization (WHO), more than 600 million adults are obese, and obesity amongst teenagers is increasingly prevalent (Jiao et al., 2019). Obesity not only affects quality of life, but also associated with numerous serious diseases, such as hypertension, type 2 diabetes mellitus, cardiovascular disease, and cancer (Gowd, Karim, Shishir, Xie, & Chen, 2019). Although there were genetic and external factors that contribute to obesity, the root cause was an imbalance between dietary intake and energy consumption (Zhang et al., 2018). While drugs can be used to enable weight loss, they typically must be taken for long periods, and have serious side effects (Dunlop & Rosenzweig-Lipson, 1998). Safer and more efficient treatments are needed in the effort to control obesity.

The human intestinal tract contains around 1014 microorganisms that form a complex and stable community (Khan et al., 2019). These gut microbiota help to maintain normal physiological host functions such as nutrition, immunity, and digestion (Kan et al., 2020). Imbalanced gut microbiota may lead to a variety of chronic diseases, the most concerning of which is obesity (Delzenne et al., 2019). A high-fat diet usually leads to obesity, but only if the gut microbiota was needed. Backhed et al. (2004) found that germ-free animals did not become obese even when fed a high-fat diet, demonstrating that gut microbiota were required for the development of obesity. In addition, the obesity phenotype could be transferred from obese to non-obese mice by transplantation of gut microbiota (Turnbaugh et al., 2006). Fei and Zhao (2013) identified Enterobacter cloacae B29 as one of the leading culprits in obesity, demonstrating for the first time a direct causal relationship between gut microbiota and obesity. However, obesity also significantly affects the diversity and structure of the gut microbiota. The gut microbiota in a normal host is always in a state of dynamic balance, while obesity can break the balance and change the diversity of the microbiota, resulting in a decrease of probiotics and an increase of harmful bacteria (Wang et al., 2014). For example, Liu et al. (2017) found that the diversity of gut microbiota in obese people was lower than that in lean people. Kan et al. (2020) classified the beneficial and harmful bacteria of obesity at the genus level, and suggested that Lactobacillus, Bacteroides, and Akkermansia were beneficial bacteria, while Oscillibacter, Marvinbryantia, and Anzerotruncus were harmful bacteria.

Polyphenols are bioactive compounds commonly found in plants. Substantial evidence suggests that polyphenols have a crucial role in attenuating obesity (Gowd et al., 2019). Recently, the effects of plant polyphenols on gut microbiota and the incidence of obesity have attracted extensive attention (Correa, Rogero, Hassimotto, & Lajolo, 2019). Polyphenols can increase the numbers of beneficial bacteria and inhibit the growth of pathogens (Mosele, Macia, & Motilva, 2015). Conversely, gut microbiota may also affect polyphenol metabolism and improve polyphenol bioavailability (Zhang, Zhu, Yang, Huang, & Ho, 2021). The major commercially available sources of plant polyphenols are tea and grape seed polyphenols, both of which are reported to have anti-obesity activity. Zhang et al. (2018) reported that green tea polyphenols promoted the growth of beneficial microflora and improved the diversity of gut microbiota, resulting in an anti-obesity effect. Seo, Kim, Jeong, Yokoyama, and Kim (2017) found that grape seed polyphenol extracts could modulate body weight and plasma lipid concentrations in high-fat mice by affecting gut microbiota. However, the raw materials that are typically used to prepare plant polyphenols are limited by high costs and other factors. Researchers have therefore sought alternative sources that are rich in polyphenols and are available at low cost.

Thinned peach fruit is a by-product of commercial peach production and is generated in high quantities at 100 kg/acre (Wei et al., 2021). Thinned peaches are 10-fold richer in polyphenols than mature fruit (Guo et al., 2020). Our previous study showed that thinned peach polyphenols (TPP) had excellent antioxidant, hypoglycemic, and hypolipidemic activities in vitro; they contained chlorogenic acid, neochlorogenic acid, and catechin as primary components, and were free of harmful compounds, such as amygdalin (Dai et al., 2022). We hypothesize that TPP may have anti-obesity effects, and other researchers reported that polyphenols obtained from other thinned fruit have anti-obesity effects, such as apples (Azuma, Osada, Aikura, Imasaka, & Handa, 2013) and Rubus coreanus (Kim et al., 2020). Jo et al. (2017) found that the anti-obesity activity of polyphenols from unripe Cudrania tricuspidata fruit was higher than of polyphenols from ripe fruit. However, thinned peach polyphenols have not been examined as thoroughly as other plant polyphenols for anti-obesity properties, and the relationship between thinned peach polyphenols and gut microbiota has not yet been investigated.

The purpose of this study was to investigate the anti-obesity effects of TPP on mice using analyses that included body weight, serum biochemistry, and liver histopathology. The 16S rRNA amplicon sequencing technology was also conducted to study the effects of TPP on the gut microbiota in mice fed a high-fat diet. The interrelationship between anti-obesity effects and gut microbiota was examined to provide theoretical support for the application of TPP in the prevention and treatment of obesity.

Section snippets

Preparation of TPP

Thinned peaches (Prunus persica L. cv. Hujingmilu) were collected 25 d after blossoming in Fenghua, Ningbo, Zhejiang Province, China. TPP was prepared as described in our previous study (Dai et al., 2022). Briefly, 5 g of thinned peach tissue was subjected to ultrasonic-assisted extraction (147 W) in 180 mL ethanol (70 %) for 25 min at 50 ℃. Polyphenols were then purified using NKA-9 resin. The purified material was freeze-dried and stored at −80 ℃.

Animal experiments

The animal experiment was designed as

Effect of TPP on body weight, food intake, and water intake in mice

The effect of TPP on body weight in mice are shown in Fig. 1. HFD mice were markedly larger in appearance than LFD mice by the end of the experiment (Fig. 1A) and had significantly higher average body weights (Fig. 1B). As expected, the body weight growth rate for mice in HFD group was higher than the corresponding rate in the LFD group. However, TPP treatment in mice fed a high-fat diet resulted in reduced weight gain rate to an intermediate value between the HFD and LFD groups. By the 5th

Discussion

Evidence suggests that peach polyphenols may affect obesity in several ways. Kan et al. (2020) found that peach peel polyphenols reduced serum lipid levels (TC, TG, LDL-C) in obese mice in a dose-dependent manner, and a dietary supplement derived from peach peel polyphenols improved liver histopathology in mice (hepatic steatosis and vesicular degeneration). Rodriguez-Gonzalez et al. (2018) suggest that polyphenols in peach juice decreased triglyceride levels in serum and prevent steatosis.

Conclusion

In summary, in mice fed a high-fat diet, TPP feeding results in reduced obesity, obesity-related liver pathology, and levels of TC, TG, LDL-C, ASL, and ALT, and increased levels of HDC-C. These effects are associated with changes in the gut microbiota of high-fat mice, which become more diverse as TTP feeding continues. TPP promotes the growth of probiotics (such as Alistipes, Akkermansia, Klebsiella, and Bacteroides) and inhibits increases in harmful bacteria (including Helicobacter and

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We gratefully acknowledge support from the Zhejiang Key R & D Program of China (award 2020C02037) and the Ningbo Agricultural Research Project of China (award 2021S064).

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