Evaluation of antiobesogenic properties of fermented foods: In silico insights
发酵食品抗肥胖特性的评估：计算机见解

Abdullahi Adekilekun Jimoh | Oluwafemi Ayodeji Adebo
阿卜杜拉希·阿德基勒昆·吉莫 |奥卢瓦费米·阿约德吉·阿德博

Centre for Innovative Food Research (CIFR), Department of Biotechnology and Food Technology, Faculty of Science, University of Johannesburg, Doornfontein, Johannesburg, South Africa
南非约翰内斯堡多恩方丹约翰内斯堡大学理学院生物技术与食品技术系创新食品研究中心

Correspondence 通信

Oluwafemi Ayodeji Adebo, Centre for Innovative Food Research (CIFR), Department of Biotechnology and Food Technology, Faculty of Science, University of Johannesburg, Doornfontein, Johannesburg 2094, South Africa. Email: oaadebo@gmail.com; oadebo@uj.ac.za
Oluwafemi Ayodeji Adebo，约翰内斯堡大学理学院生物技术与食品技术系创新食品研究中心（CIFR），约翰内斯堡多伦方丹 2094，南非。电子邮件：oaadebo@gmail.com;oadebo@uj.ac.za

Funding information 资金信息

South African Medical Research Council; National Research Foundation of South Africa, Grant/Award Number: SRUG2204285188; University of Johannesburg
南非医学研究委员会;南非国家研究基金会，资助/奖励编号：SRUG2204285188;约翰内斯堡大学

Abstract 抽象

Obesity prevalence has steadily increased over the past decades. Standard approaches, such as increased energy expenditure, lifestyle changes, a balanced diet, and the use of specific drugs, are the conventional strategies for preventing or treating the disease and its associated complications. Fermented foods and their subsequent bioactive constituents are now believed to be a novel strategy that can complement already existing approaches for managing and preventing this disease. Recent developments in systems biology and bioinformatics have made it possible to model and simulate compounds and disease interactions. The adoption of such in silico models has contributed to the discovery of novel fermented product targets and helped in testing hypotheses regarding the mechanistic impact and underlying functions of fermented food components. From the studies explored, key findings suggest that fermented foods affect adipogenesis, lipid metabolism, appetite regulation, gut microbiota composition, insulin resistance, and inflammation related to obesity, which could lead to new ways to treat these conditions. These outcomes were linked to probiotics, prebiotics, metabolites, and complex bioactive substances produced during fermentation. Overall, fermented foods and their bioactive compounds show promise as innovative tools for obesity management by influencing metabolic pathways and overall gut health.
在过去的几十年里，肥胖患病率稳步上升。标准方法，例如增加能量消耗、改变生活方式、均衡饮食和使用特定药物，是预防或治疗该疾病及其相关并发症的常规策略。发酵食品及其随后的生物活性成分现在被认为是一种新颖的策略，可以补充现有的管理和预防这种疾病的方法。系统生物学和生物信息学的最新发展使得对化合物和疾病相互作用进行建模和模拟成为可能。采用这种计算机模型有助于发现新的发酵产品靶标，并有助于检验有关发酵食品成分的机制影响和潜在功能的假设。从探索的研究中，主要发现表明发酵食品会影响脂肪生成、脂质代谢、食欲调节、肠道微生物群组成、胰岛素抵抗和与肥胖相关的炎症，这可能会带来治疗这些疾病的新方法。这些结果与发酵过程中产生的益生菌、益生元、代谢物和复杂的生物活性物质有关。总体而言，发酵食品及其生物活性化合物通过影响代谢途径和整体肠道健康，显示出作为肥胖管理创新工具的前景。

KEYWORDS 关键字

fermentation, health benefits, in silico, molecular dynamics simulation, obesity
发酵，健康益处，计算机，分子动力学模拟，肥胖

1 | INTRODUCTION 1 |介绍

Obesity, a key global public health concern today, is a result of excessive accumulation of excess adipose tissue (Khan et al., 2021) that affects nearly every organ system. Obesity is thought to be a major contributing factor to several chronic-related non-communicable diseases (NCDs)
肥胖是当今全球一个关键的公共卫生问题，是多余脂肪组织过度积累的结果（Khan 等人，2021 年），几乎影响了每个器官系统。肥胖被认为是多种慢性相关非传染性疾病（NCD）的主要促成因素
(Canfora et al., 2019; Marzullo et al., 2020). As per the WHO, obesity and overweight account for at least 2.8 million deaths annually (WHO, 2021, 2023). Recent studies have reported that more than 1 billion people in the world are living with this NCD (Phelps et al., 2024; Ruze et al., 2023). To date, all nations are affected by obesity, and within the next 10 years, this is expected to become even
（Canfora 等人，2019 年;Marzullo 等人，2020 年）。根据世界卫生组织的数据，肥胖和超重每年至少导致 280 万人死亡（世界卫生组织，2021 年，2023 年）。最近的研究报告称，世界上有超过 10 亿人患有这种非传染性疾病（Phelps 等人，2024 年;Ruze 等人，2023 年）。迄今为止，所有国家都受到肥胖的影响，预计在未来 10 年内，肥胖率将趋于平稳

more pronounced, leading to a greater number of years lost from a healthy life, disability, and death. Therefore, it is critical to take swift action to prevent and treat the prevalence of obesity and its associated metabolic comorbidities (Ruze et al., 2023).
更明显，导致因健康生活、残疾和死亡而损失的年数更多。因此，迅速采取行动预防和治疗肥胖及其相关代谢合并症的患病率至关重要（Ruze 等人，2023 年）。

The spectrum of newly developed medical gadgets, pharmacology, lifestyle therapies, and increasingly popular and advanced bariatric operations are among the therapeutic alternatives available today for managing and treating obesity. Although endoscopic and non-endoscopic surgical procedures have become popular among obese patients, they are still far from perfect due to the inherent risks and complications (Lingvay et al., 2022; Ruze et al., 2023). People frequently use antiobesity medications to avert and cure obesity and associated complications; however, a variety of side effects have prompted the need for safe and efficient natural product alternatives (Jalili et al., 2023). In this case, there is a need to enhance the worldwide population’s diet with food products that can combat obesity and other NCDs while boosting a person’s health condition. Functional foods or healthy foods (e.g., fermented foods) specially developed and formulated to address chronic illnesses and offer health benefits can partially bridge the gap among drugs, pharmaceuticals, and food, potentially offering therapeutic or disease-prevention benefits (Misra et al., 2021; Oladimeji & Adebo, 2024; Xiao et al., 2023).
一系列新开发的医疗设备、药理学、生活方式疗法以及日益流行和先进的减肥手术是当今可用于管理和治疗肥胖的治疗替代方案之一。尽管内窥镜和非内窥镜外科手术在肥胖患者中越来越受欢迎，但由于固有的风险和并发症，它们仍然远非完美（Lingvay 等人，2022 年;Ruze 等人，2023 年）。人们经常使用抗肥胖药物来避免和治疗肥胖和相关并发症;然而，各种副作用促使需要安全高效的天然产品替代品（Jalili 等人，2023 年）。在这种情况下，需要通过能够对抗肥胖和其他非传染性疾病的食品来改善全世界人口的饮食，同时改善一个人的健康状况。专门为解决慢性病和提供健康益处而开发和配制的功能性食品或健康食品（例如发酵食品）可以部分弥合药物、药品和食品之间的差距，从而可能提供治疗或疾病预防益处（Misra 等人，2021 年;Oladimeji 和 Adebo，2024 年;Xiao 等人，2023 年）。

Fermented foods are those that undergo transformation through the process of fermentation, in which microorganisms such as bacteria, molds, or yeasts thrive and catalyze enzymatic changes in the food’s components. This microbial activity and subsequent metabolism alter the texture, flavor, and nutritional profile of the food, resulting in unique and often enhanced characteristics (Adebo, 2020; Dimidi et al., 2019). The majority of fermented foods have been shown to prevent obesity, including cabbageapple juice (Park et al., 2020), douche (An et al., 2022), probiotic-fermented blueberry juice (Zhong et al., 2020), huyou juice (Yan et al., 2020), wine pomace (Gerardi et al., 2020), ougan juice (Guo et al., 2021), and Gochujang (Son et al., 2020). Moreover, fermented foods, which are rich in probiotics, prebiotics, and postbiotics, have shown promising results in modulating gut microbiota, improving metabolic health, and reducing obesity-related inflammation (Jalili et al., 2023). However, obesity is a complicated, multifaceted disease and thus necessitates comprehensive evaluation methods (Lin & Li, 2021).
发酵食品是那些通过发酵过程进行转化的食品，其中细菌、霉菌或酵母等微生物繁殖并催化食品成分的酶促变化。这种微生物活动和随后的新陈代谢改变了食物的质地、风味和营养成分，从而产生独特且通常增强的特性（Adebo，2020 年;Dimidi 等人，2019 年）。大多数发酵食品已被证明可以预防肥胖，包括卷心菜苹果汁（Park 等人，2020 年）、冲洗剂（An 等人，2022 年）、益生菌发酵蓝莓汁（Zhong 等人，2020 年）、胡油汁（Yan 等人，2020 年）、酒渣（Gerardi 等人，2020 年）、欧干汁（Guo 等人，2021 年）和辣椒酱（Son 等人，2020 年）。此外，富含益生菌、益生元和后生元的发酵食品在调节肠道微生物群、改善代谢健康和减少肥胖相关炎症方面显示出有希望的结果（Jalili 等人，2023 年）。然而，肥胖是一种复杂、多方面的疾病，因此需要综合评估方法（Lin & Li，2021）。

In silico approaches, involving computational simulations and bioinformatics tools, offer a robust platform for the preliminary assessment of the antiobesogenic properties of fermented foods. These methods can predict the interactions between bioactive compounds and molecular targets involved in obesity pathways, thus providing
计算机方法涉及计算模拟和生物信息学工具，为初步评估发酵食品的抗肥胖特性提供了一个强大的平台。这些方法可以预测生物活性化合物与肥胖途径中涉及的分子靶点之间的相互作用，从而提供
insights into the potential mechanisms of action. By integrating data from various biological databases, in silico evaluations can identify candidate compounds and prioritize them for further experimental validation (de Medeiros et al., 2024). In nutritional studies such as this, in silico approaches can analyze large datasets and significantly reduce the financial burden associated with traditional experimental research by simulating experiments and predicting outcomes without the need for physical resources (Duarte et al., 2023). In silico approaches minimize the need for animal testing and enable human model simulation by addressing ethical concerns. Additionally, by enabling personalized nutrition strategies and predictive analytics, these models contribute to the development of tailored dietary interventions, ultimately improving public health outcomes.
深入了解潜在的作用机制。通过整合来自各种生物数据库的数据，计算机评估可以识别候选化合物并优先考虑它们以进行进一步的实验验证（de Medeiros 等人，2024 年）。在此类营养研究中，计算机方法可以分析大型数据集，并通过模拟实验和预测结果来显着减轻与传统实验研究相关的财务负担，而无需物理资源（Duarte 等人，2023）。计算机方法最大限度地减少了动物试验的需要，并通过解决伦理问题实现人体模型模拟。此外，通过实现个性化营养策略和预测分析，这些模型有助于开发量身定制的饮食干预措施，最终改善公共卫生结果。

This review aims to provide an overview of the in silico techniques employed in the evaluation of the antiobesogenic properties of fermented foods. It will discuss the key bioactive components identified in fermented foods, their predicted molecular targets, and the potential mechanisms by which they may exert antiobesogenic effects. Furthermore, it highlights the advantages and limitations of in silico methods and suggests future directions for integrating these approaches with experimental studies to develop effective antiobesogenic interventions.
本综述旨在概述用于评估发酵食品抗肥胖特性的计算机技术。它将讨论发酵食品中鉴定的关键生物活性成分、它们预测的分子靶标以及它们可能发挥抗肥胖作用的潜在机制。此外，它还强调了计算机方法的优点和局限性，并提出了将这些方法与实验研究相结合以开发有效的抗肥胖干预措施的未来方向。

2 | FERMENTED FOODS, BIOACTIVE COMPOUNDS, AND OBESITY MANAGEMENT
2 |发酵食品、生物活性化合物和肥胖管理

Today, thousands of fermented foods and beverages are consumed due to various food matrix and microbe combinations. They are classified using different approaches, with one of the most prevalent methods being based on the type of raw materials used (plant or animal sources), fermentation type (e.g., back-slopped, spontaneous, or starter culture), and form of fermentation (solid state or submerged). Consequently, fermented foods have been grouped into categories such as vegetables/fruits, cereals, legumes, roots/tubers, dairy, fish/meat, alcoholic beverages, and others. Of these groups, there is limited research available on the impacts of fermented meat and fish on obesity, as these products from their fermentation often contain high levels of salt, preservatives, and other additives. Thus, a detailed summary of various fermented foods, processing methods, models, and associated antiobesogenic effects is presented in Table 1.
今天，由于各种食物基质和微生物组合，数以千计的发酵食品和饮料被消费。它们使用不同的方法进行分类，最流行的方法之一是基于所用原材料的类型（植物或动物来源）、发酵类型（例如，后倾、自发或发酵剂）和发酵形式（固态或浸没）。因此，发酵食品被分为蔬菜/水果、谷物、豆类、根茎/块茎、乳制品、鱼/肉、酒精饮料等类别。在这些群体中，关于发酵肉和鱼对肥胖影响的研究有限，因为这些发酵产品通常含有高含量的盐、防腐剂和其他添加剂。因此，表1详细总结了各种发酵食品、加工方法、模型和相关抗肥胖作用。

Fermented foods contain beneficial microbes (potential probiotics) that synergistically interact with prebiotics, which act as food for the probiotics and promote their growth. This further enables them to perform their
发酵食品含有有益微生物（潜在的益生菌），可与益生元协同相互作用，益生元作为益生菌的食物并促进其生长。这进一步使他们能够执行

TABLE 1 Selected fermented food groups and their specific use in obesity management.
表1 选定的发酵食品组及其在肥胖管理中的具体用途。

Fermented food products 发酵食品	Processing method 加工方法	Models 模型	Specific antiobesogenic effect 特异性抗肥胖作用	References 引用
Fermented dairy products 发酵乳制品
Milk 牛奶	Fermentation using LAB 使用 LAB 发酵	In vitro using 3T3-L1 preadipocyte, in silico digestion 使用 3T3-L1 前脂肪细胞进行体外消化	Inhibit pancreatic lipase 抑制胰脂肪酶	ManzanarezQuin et al. (2023) ManzanarezQuin 等人（2023）
Milk 牛奶	Fermentation by Lactobacillus plantarum Q180 植物乳杆菌 Q180 发酵	Murine 3T3-L1 preadipocyte 小鼠 3T3-L1 前脂肪细胞	Inhibit pancreatic lipase 抑制胰脂肪酶	Kim and Lim (2020) 金和林（2020）
Kefir 克非尔	Fermentation by Lactobacillus spp., Yeast spp. 由乳酸杆菌属、酵母属发酵。	Asymptomatic overweight adults 无症状超重成人	Improvement in serum zonulin level and general mood of the participants 血清连蛋白水平和参与者总体情绪的改善	Pražnikar et al. (2020) Pražnikar 等人（2020）
		Wistar female rats Wistar 雌性大鼠	Reduced low-density lipoprotein by $24 % - 66 %$ , raised blood glucose by $36 %$ , and enhanced high-density lipoprotein by $32 %$ in rats 在大鼠 $32 %$ 中降低低密度脂蛋白 $24 % - 66 %$ ，提高血糖 $36 %$ ，增强高密度脂蛋白	Tiss et al. (2020) 蒂斯等人（2020）
		Male C57BL/6 mice 公 C57BL/6 小鼠	Decreased weight gain and changes in both the gut microbiota and mycobiota. The kefir administration lowers blood cholesterol and ameliorates systemic inflammation in HFD-fed mice 减少体重增加和肠道微生物群和真菌群的变化。开菲尔给药可降低血液中的胆固醇并改善 HFD 喂养小鼠的全身炎症	Kim et al. (2014), Kim, Kim, et al. (2017) Kim 等人（2014）、Kim， Kim 等人（2017）
		Male C57BL/6J mice 公 C57BL/6J 小鼠	Reduce the buildup of intracellular lipids and epididymal adipose tissue by 19% and body weight gain. Upregulation of PPAR- $α$ in adipose tissue and reduction of cholesterol 减少细胞内脂质和附睾脂肪组织的堆积 19% 和体重增加。上调脂肪组织中 PPAR- $α$ 和降低胆固醇	Kim, Jeong, et al. (2017), Lim et al. (2017) Kim， Jeong， et al. （2017）， Lim et al. （2017）
Fermented tea/herbs 发酵茶/香草
Chinese dark tea 中国黑茶	Extraction, fermentation with Aspergillus niger, and pasteurization 提取、黑曲霉发酵和巴氏杀菌	Male C57BL/6 mice 公 C57BL/6 小鼠	Inhibited mice from gaining weight or visceral fat and controlled the expression of genes linked to obesity 抑制小鼠体重或内脏脂肪增加，并控制与肥胖相关的基因的表达	Sun et al. (2019) 孙等人（2019）
Fermented RAM 发酵内存	Fermentation by $L$ . plantarum 发酵方式 $L$ 。植物	Male Sprague-Dawley rats 雄性 Sprague-Dawley 大鼠	Fermented RAM's anti-obesity effects are shown by preventing endotoxemia and related inflammation, influencing the distribution of intestinal microflora, and suppressing adipogenesis 发酵 RAM 的抗肥胖作用体现在预防内毒素血症和相关炎症、影响肠道菌群分布和抑制脂肪生成	Wang et al. (2015) 王等人（2015）
Fu brick tea 福砖茶	Microbial-fermented tea 微生物发酵茶	Male Sprague-Dawley rats 雄性 Sprague-Dawley 大鼠	The fermented tea influenced intestinal barrier activities while lowering inflammation and oxidative stress. Additionally, it raises the gut microbiota's Firmicutes to Bacteroidetes ratio 发酵茶影响肠道屏障活动，同时降低炎症和氧化应激。此外，它还提高了肠道微生物群的厚壁菌门与拟杆菌门的比率	Zhou et al. (2021) 周等人（2021）
Fermented tea 发酵茶	Natural fermentation 自然发酵	Male C57BL/6N mice 雄性 C57BL/6N 小鼠	Significant reductions in body weight and adipocyte lipid accumulation 体重和脂肪细胞脂质积累显着减少	Lee et al. (2024) Lee 等人（2024）
Fermented vegetables/fruits/beverage 发酵蔬菜/水果/饮料
Ginseng vinegar 人参醋	Two-stage fermentation by different microbial strains 不同微生物菌株的两阶段发酵	Male C57/BL6 mice 雄性 C57/BL6 小鼠	Triglycerides, total cholesterol, epididymal fat weight, and body weight gain were all considerably decreased by the addition of ginseng vinegar product 甘油三酯、总胆固醇、附睾脂肪重量和体重增加均因人参醋制品的添加而显着降低	Oh et al. (2019) Oh 等人（2019）
Cabbage-apple juice 卷心菜苹果汁	Fermentation by $L$ . plantarum EM 发酵方式 $L$ 。植物 EM	Sprague-Dawley rats Sprague-Dawley 大鼠	Consuming fermented cabbage-apple juice regulates liver weight and overall body weight 食用发酵卷心菜苹果汁可以调节肝脏重量和整体体重	Park et al. (2020) Park 等人（2020）
Red wine pomace product 红酒渣制品	Vinification of Vitis vinifera L. cv 葡萄 L. cv 的酿造	Male Wistar rats 雄性 Wistar 大鼠	Decreased lipid deposition, blood sugar, liver weight, and obesity-related problems while boosting antioxidant status 减少脂质沉积、血糖、肝脏重量和肥胖相关问题，同时提高抗氧化状态	Gerardi et al. (2020) 杰拉尔迪等人（2020）

Fermented food products Processing method Models Specific antiobesogenic effect References Fermented dairy products Milk Fermentation using LAB In vitro using 3T3-L1 preadipocyte, in silico digestion Inhibit pancreatic lipase ManzanarezQuin et al. (2023) Milk Fermentation by Lactobacillus plantarum Q180 Murine 3T3-L1 preadipocyte Inhibit pancreatic lipase Kim and Lim (2020) Kefir Fermentation by Lactobacillus spp., Yeast spp. Asymptomatic overweight adults Improvement in serum zonulin level and general mood of the participants Pražnikar et al. (2020) Wistar female rats Reduced low-density lipoprotein by 24%-66%, raised blood glucose by 36%, and enhanced high-density lipoprotein by 32% in rats Tiss et al. (2020) Male C57BL/6 mice Decreased weight gain and changes in both the gut microbiota and mycobiota. The kefir administration lowers blood cholesterol and ameliorates systemic inflammation in HFD-fed mice Kim et al. (2014), Kim, Kim, et al. (2017) Male C57BL/6J mice Reduce the buildup of intracellular lipids and epididymal adipose tissue by 19% and body weight gain. Upregulation of PPAR- alpha in adipose tissue and reduction of cholesterol Kim, Jeong, et al. (2017), Lim et al. (2017) Fermented tea/herbs Chinese dark tea Extraction, fermentation with Aspergillus niger, and pasteurization Male C57BL/6 mice Inhibited mice from gaining weight or visceral fat and controlled the expression of genes linked to obesity Sun et al. (2019) Fermented RAM Fermentation by L. plantarum Male Sprague-Dawley rats Fermented RAM's anti-obesity effects are shown by preventing endotoxemia and related inflammation, influencing the distribution of intestinal microflora, and suppressing adipogenesis Wang et al. (2015) Fu brick tea Microbial-fermented tea Male Sprague-Dawley rats The fermented tea influenced intestinal barrier activities while lowering inflammation and oxidative stress. Additionally, it raises the gut microbiota's Firmicutes to Bacteroidetes ratio Zhou et al. (2021) Fermented tea Natural fermentation Male C57BL/6N mice Significant reductions in body weight and adipocyte lipid accumulation Lee et al. (2024) Fermented vegetables/fruits/beverage Ginseng vinegar Two-stage fermentation by different microbial strains Male C57/BL6 mice Triglycerides, total cholesterol, epididymal fat weight, and body weight gain were all considerably decreased by the addition of ginseng vinegar product Oh et al. (2019) Cabbage-apple juice Fermentation by L. plantarum EM Sprague-Dawley rats Consuming fermented cabbage-apple juice regulates liver weight and overall body weight Park et al. (2020) Red wine pomace product Vinification of Vitis vinifera L. cv Male Wistar rats Decreased lipid deposition, blood sugar, liver weight, and obesity-related problems while boosting antioxidant status Gerardi et al. (2020)

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Evaluation of antiobesogenic properties of fermented foods: In silico insights 发酵食品抗肥胖特性的评估：计算机见解