Abstract
Objectives
Fruit vinegar is one of the most famous fruit byproducts worldwide with several unique properties. There are two types of fruit vinegar, artisanal and industrial, for consumers to choose from. This review aims to assess for the first time the phytochemistry of fruit vinegar and its anti-inflammatory effects.
Method
The present work was conducted based on a literature search that selected the relevant papers from indexed databases such as Scopus, Science Direct, MDPI, PubMed, Hindawi, and Web of Science. We used numerous terms to assure a good search in different databases, including fruit vinegar, phytochemistry, bioavailability and bioaccessibility, and anti-inflammatory effect. All articles were selected based on their relevance, quality, and problematic treatment.
Results
Literature data have shown that vinegar has a long medicinal history and has been widely used by different civilizations, due to its richness in bioactive molecules, vinegar plays an important role in the prevention and treatment of various inflammatory diseases, including atopic dermatitis, mastitis, asthma, arthritis, acute pancreatitis, and colitis. Fruit vinegar consumption benefit is highly dependent on its chemical composition, especially organic acids and antioxidants, which can act as nutraceuticals.
Conclusion
Fruit vinegar has a rich chemical composition, including organic acids that can be transformed in the digestive system into compounds that play an important role in health-promoting features such as anti-inflammatory effects throughout the control of intestinal microbiota and pro-inflammatory cytokine production.
Graphical abstract
Supplementary Information
The online version contains supplementary material available at 10.1007/s40199-023-00493-9.
Keywords: Fruit vinegar, Phytochemistry, Anti-inflammatory effect, Antioxidant effect
Introduction
Fruit vinegar is a successful and diverse fruit-byproduct distributed worldwide and used by different civilizations across the world. It is very difficult to determine the exact time of its first use but it appears in several ancient writings in early times as a natural medication for several diseases [1]. Formally, the emergence of vinegar accompanied the discovery of fermentation from fruits and other sugar sources [2]. On the basis of the long medical history of this popular product, several experimental studies have been conducted to confirm its medicinal uses such as antidiabetic effect [3], neuroprotective effect [4], hepatoprotective effect [5, 6], anticancer effect [7], cardioprotective effect [8, 9], immunomodulatory effect [10], osteoprotective effect [11], and anti-inflammatory effect [12, 13]. Fruit vinegar consumption is beneficial for both animal and human health-related to its dense chemical composition [14]. Fruit vinegar is an excellent natural source of bio-valuable molecules, including phenolic compounds, flavonoids, tannins, melanoidins, tetramethylpyrazine, organic acids, and vitamins [15]. These molecules act their tremendous properties throughout pleiotropy effects. The bioactive compounds of fruit vinegar act as preventive agents against peroxidation of DNA, proteins, and lipids, which plays an important role in aging, cell proliferation, neurodegenerative disorders, and failure of the antioxidant defense system [16, 17]. Importantly, the chemical complexity of vinegar boosts the antioxidant defense system to attenuate the deleterious effects of toxic agents and reactive oxygen species (ROS) [18]. ROS disrupt various physiological activities in humans and induce different disorders such as inflammation throughout the activation of tissue tumor necrosis factor (TNF-α) and liberation of proinflammatory mediators [19]. Growing evidence has shown that the administration of fruit vinegar ameliorates intestinal permeability and controls intestinal microbiota, thereby inhibiting the entry of harmful molecules into the blood stream and controlling the inflammation process [12, 20, 21]. Additionally, numerous studies have shown that the consumption of fruit vinegar controls the production of proinflammatory cytokines [8, 10, 12, 16, 20].
The wicker in the history of fruit vinegar assures us that this product is widely used in folk medicine dating back to antiquity. The Egyptians were probably the first to discover and use vinegar under the name of Hmd or Hemedj [2]. The Babylonians used vinegar as a condiment and preservative. In Muslim culture, the meaning of vinegar has been established according to the Hadith narrated by Aisha ‘May Allah be pleased with her’ may the Prophet, may the peace and blessing of God be upon him, said ‘’The best of condiment is vinegar’’ [22]. He also said (Blessing and peace of Allah be upon him)’’ may Allah most high bless the vinegar because it was the sauce of the prophets before me’’ as reported by Ibn Madja (3318) and Dhaif al-Jami (5973). In his book called ‘’ Al-Quanon fi Tibb’’, the law of medicine’’ by Ibn Sina or Avicenna (980–1037) also mentioned the following properties of vinegar: coagulation, soothing headaches, expectorant, and healing of burns and skin inflammation [2].
To the best of our knowledge, there is no article review that summarizes and discusses the capacity of fruit vinegar to manage and regulate inflammatory disorders. Therefore, the main objective of the current review was to summarize the overview of fruit vinegar, including phytochemistry, bioavailability, bioaccessibility, and anti-inflammatory effects, to acquire a better understanding of the potential anti-inflammatory abilities of fruit vinegar.
Methodology
The present work was conducted based on the literature search that selected the relevant papers available in indexed databases such as Scopus, Science Direct, MDPI, PubMed, Hindawi, and Web of Science. We used numerous terms to assure a good search in different databases used including fruit vinegar, phytochemistry, bioavailability and bioaccessibility, and anti-inflammatory effect. All articles were selected based on their relevance, quality, and problematic treatment.
The studies used to create the current study were chosen on the basis of their relevancy, including scientific literature that alluded to the phytochemistry and anti-inflammatory characteristics of fruit vinegar. Other studies on the biological characteristics of fruit vinegar were excluded. The study’s search was limited to articles published exclusively in English.
Phytochemistry of fruit vinegar
Fruit vinegar is a very popular product with different chemical and aroma profiles [15]. The separation and purification of chemicals are performed using different techniques, such as gas chromatography, high-performance liquid chromatography, paper chromatography, thin-layer chromatography, ion exchange chromatography, gel permeation chromatography, affinity chromatography, and mass spectrometry [23]. A wide range of bioactive compounds are detected in fruit vinegars, including phenolic acids, flavonoids, melanoidins, tetramethylpyrazine, and organic acids. The phytochemistry profile of fruit vinegar is highly related to the nature of raw materials, fermentation method, microorganisms, fermentation time, and aging [24]. High amounts of polyphenolics are present in fruit vinegar varying between 252.90 ± 3.90 and 681.73 ± 14.55 mg GAE/L for grape vinegar, 119.16 ± 1.66 mg GAE/100mL for cherry vinegar; 100 ± 8.41 mg GAE/100 mL for peach vinegar, 106.91 ± 1.64 mg GAE/100mL for apple vinegar, 99 ± 2 mg GAE/100mL for raspberry vinegar, 124 ± 5 mg GAE/100mL for blueberry vinegar, 170 ± 8 mg GAE/100mL for blackberry vinegar, 2020 ± 24 mg GAE/100mL for rose hip vinegar, and 44 ± 2 mg GAE/100mL for persimmon vinegar [25–27]. These molecules are represented by transferulic acid for apple and cherry vinegars (43.921% and 29.88%, respectively) [25, 28], arbutin (77.16%) for cherry vinegar [25]. The determination of the phenolic profile of three types of fruit vinegar (Cherries vinegar, peaches vinegar, and apples vinegar) available on the market revealed 43 compounds with an abundance of arbutin, transferulic acid, apigenin, and ferulic acid [25]. Other researchers found that chlorogenic acid, gallic acid, catechin, and caffeic acid were the most abundant molecules in apple vinegar and pomegranate vinegar [29], whereas in persimmon vinegar and kiwifruit vinegar, gallic acid was the most active component found at high amounts [30]. The fermentation process of different raw materials used to produce vinegar affects the phenolic profile of the end product, it enhances the release of bioactive compounds, and the microorganisms involved in the process participate in the conversion of these chemicals into more active compounds, including organic acids, melanoidins, and tetramethylpyrazine [27]. Organic acids are also other types of bioactive compounds associated with health benefits against many diseases [31]. They control the vinegar aromas and can be found naturally or newly synthesized during vinegar manufacturing [32]. Acetic acid is the major component found in all kinds of fruit vinegar with proportions of 92.64 and 93.22% (29, 55). Liu et al. detected tartaric acid, malic acid, lactic acid, and succinic acid in apple, red wine, white wine, and balsamic vinegars [33].
Melanoidins are other bioactive compounds found in vinegar that play an important role in the determination of vinegar flavor [34]. In a study conducted by Liu et al. that the concentration of melanoidins in Zhenjiang aromatic vinegar ranged from 19.27 ± 20.57 to 22.57 ± 20.45 mg/mL [34]. These compounds exhibited considerable antioxidant abilities, as previously determined using ABTS and FRAP assays. The obtained values are expressed as follows: 2750.3 ± 65.2 and 1286.2 ± 679.9 mg Vitamin C/kg of balsamic vinegar, respectively [35]. Other active compounds, such as phenolic compounds, can link to melanoidins, forming complex molecules with high antioxidant potential [35].
The amounts of tetramethylpyrazine found in 36 fruit vinegar samples ranged from 0.113 ± 0.001 to 131.108 ± 1.966 mg/kg [36]. Wu et al. found that the quantity of tetramethylpyrazine detected in 9 kinds of fruit vinegar varied between 2.87 and 29.04 mg/L [37].
Bioavailability of bioactive compounds from fruit vinegar
The bioavailability of active ingredients is a critical factor in predicting their related-health benefits. It refers to the capacity of these compounds to pass through various barriers and enter the circulatory system [38, 39]. Bioactive compounds are distributed throughout the whole body via the circulatory system to act on specific targets [39]. Bakir et al. demonstrated that the in vitro digestion using pancreatin-bile salts mxiture had a significant impact on phytochemical composition of both investigated samples (grape and apple vinegars) [40]. In addition, it has been proven that the matrix limited the effect on phytocompound bioaccessibility in vitro [40]. Previously, numerous studies documented that the presence of such components accounting for citric acid and glucose strongly affects the passage of bioactive compounds over intestinal barriers [41, 42].
Mounting scientific evidence showed that the amounts of three active compounds including chlorogenic acid, caffeic acid, and quinic acid, decrease across the digestive tract and circulatory system. It was found that the amounts of molecules under study decreased significantly in plasma and urine. The bioavailability of chlorogenic acid depends on its metabolism by the gut microbiota [43]. A published study by Kishida and Matsumoto, reported that caffeic acid, p-coumaric acid, and ferulic acid are more highly predisposed to penetrate intestinal barriers than chlorogenic acid [44]. The study of the bioavailability of bioactive compounds is limited by the impracticality and ethical issues required to conduct further scientific research in vivo. For this reason, the scientific community concentrates its attention on the bioaccessibility of bioactive compounds, which is considered a key factor that controls their bioactivity [45–47]. Solid knowledge of the digestive fate of active ingredients of different vegetal matrices could be a key step in promoting health and ameliorating performance. Understanding gut-microbiota interactions with bioactive compounds of fruit vinegar could provide scientific insights into the beneficial properties of the active ingredient in question [20]. The fermentation process of fruits enhances the breaking of the vegetal matrix to release its bioactive food compounds and subsequently improves the bioaccessibility of the molecules in question [48]. The transformation of active ingredients found in esters, glycosides, or polymer forms could be a key factor in elevating the bioaccessibility of these compounds, thereby improving gastrointestinal absorption [49]. Vinegar’s chemical composition is enriched during manufacturing and aging processes, which increases the release of bioactive compounds from the raw material, thereby elevating their bioaccessibility [50, 51].
Management of inflammatory diseases by fruit vinegar
Non-pharmacological intervention using natural products and their derivatives plays an important role in the prevention and even treatment of various diseases. Recently, one of the most interesting products that has gained huge interest due to its important health benefits is fruit vinegar. Consumption of this product regularly furnishes a wide range of beneficial properties scientifically confirmed, including antidiabetic, antioxidant, cholesterol and weight lowering, immune boosting, anticancer, and antimicrobial activities [10, 35, 52–54]. Its ability to act positively and impact inflammation makes it a good candidate product for reducing the amounts of inflammatory cytokines [10, 55, 56]. Numerous studies on animal models have confirmed its potential to ameliorate inflammation by modulating the intestinal flora [12]. The intestinal microflora constitutes an effective therapeutic target for inflammatory diseases. This imbalance induces the down-expression of claudin-1, ZO-1, and occludin in gut acid secretion, which promotes intestinal permeability and facilitates the entry of toxic agents into the general circulation [57, 58]. Toxic agents activate tissue tumor necrosis factor (TNF-α) and promote the liberation of pro-inflammatory cytokines [19]. A diet enriched with fermented foods such as fruit vinegar enhances the potential probiotic effect and bioavailability of nutrients, produces antioxidants and functional ingredients, modulates intestinal flora, and controls the immune system [59]. Vinegar contains notable amounts of living and functional microorganisms and lipopolysaccharides (LPS) generated during the vinegar aging process [60, 61]. These molecules modulate macrophage function to regulate allergy, cancer, and inflammation by boosting the phagocytic effect and reinforcing the immune system [52, 61]. Mounting scientific evidence confirms that the administration of nipa vinegar affects gut microbiota, increasing Verrucomicrobia and Proteobacteriaphylum populations, controversially, decreasing the gut Firmicutes/Bacteroidetes ratio [55]. The same findings were evoked by Han et al. after consuming a fermented Korean food named Kimchi [62]. The gut microbiota of a healthy person is characterized by the abundance of beneficial bacterial genera, including Bacteroides, Lactobacillus, Akkermansia, and Parabacteroides, whereas the lowest Blauti and Allobaculum were found in the lowest quantities [62, 63]. The presence of mucin-degrading Akkermansia is negatively correlated with the inflammatory process [64]. Fruit vinegar-derived bioactive compounds are components naturally found in raw matter or newly synthesized and secreted during the vinegar manufacturing process [65]. These active ingredients feature various chemicals, including phenolic compounds, flavonoids, tannins, organic acids, melanoidins, and tetramethylpyrazine [66]. Previous reports have shown that the organic acids of vinegars regulate the intestinal flora by controlling the digestive pH, boosting pancreatic activity, and exerting a trophic effect on the innermost layer of the gastrointestinal tract [67]. In addition, organic acids inhibit the attachment and colonization of pathogenic and invasive microorganisms [68], and ameliorate intestinal morphology and barrier function [69]. A study conducted by Jiang et al. found that treatment with vinegar improved detachment of lamina propia of the intestinal mucosa, inflammatory cell infiltration in the intestinal wall decreases p65 and ICAM-1 expression, and increased E-cadherin in the intestinal tract of rats intoxicated by Euphorbia kansui [70]. Furthermore, the regulation of the intestinal microbiota improves the production process of short-chain fatty acids (SCFA) implicated in the control of the inflammatory processes involved in numerous diseases [71]. The abundance of SCFA has a profound influence on human health throughout the upkeep of the gut-barrier task. This beneficial property has been supported by experimental evidence showing that both SCFA accounting for butyrate and propionate induce the differentiation of T-regulatory cells, which is implicated in the control of intestinal inflammation by inhibiting histone deacetylation [72, 73]. SCFA have an important protective effect against high-fat diet-induced metabolic disorders via AMP-activated protein kinase [74], or mitogen-activated protein kinase [75]. Mounting scientific evidence has shown that the consumption of fruit vinegar regularly reduces the inflammatory cytokines, cyclooxygenase (COX)-2, nitric oxide (NO), inducible nitric oxide synthase (iNOS), and mitogen-activated protein kinase (MAPKs) (Fig. 1) [56, 76–78].
Fig. 1.
Beneficial effects of fruit vinegar and possible mechanism of action involved
Atopic dermatitis
Atopic dermatitis (AD) is a skin disorder affects approximately 20% and 6% of children and adults, respectively [79]. It is characterized by the modification of skin properties, which leads to the development of bacterial infections, particularly Staphylococcus aureus [80]. This change reduces the filaggrin production process and plays an important role in epidermal acidification [81, 82]. The control of skin pH is the most common approach to restore skin equilibrium and eradicate the pathogenic microbes that are involved in AD-like S. aureus [83]. Acidifier baths using dilute bleach are employed as a therapy for AD with promising results because of their ability to destroy pathogenic microbes [84]. Bleach’s treatment is a pH standpoint strategy to handle Staphylococcus aureus, showing an effective effect compared with water baths alone [85]. However, the effectiveness and safety of bleach baths have been called into question because of their side effects [86]. The required concentration of sodium hypochlorite (0.03%) to annihilate S. aureus is considered toxic to human cells [87, 88]. Among natural remedies, vinegar appears to be a prominent natural product with double benefits, acidifier, and sanitizer [89]. The study conducted by Luu et al. showed that the treatment of patients with dilute apple cider vinegar at a dose of 0.5% acetic acid, has no significant impact on the skin barrier integrity, despite a decreasing tendency of pH and an increasing tendency of transepidermal water loss [83, 90]. In contrast, oak wood vinegar (OWV) showed an effective anti-inflammatory effect on 2,4-dinitrochlorobenzene-induced contact dermatitis in an animal model. It was also revealed that OWV suppressed IgE production, iNOS expression, and immune cell infiltration throughout STAT3 inactivation [78]. The treatment of Oxazolone-intoxicated mice ((Ox)-AD) with acidic vinegar creams reduced AD-like lesions, lowered eczema scores, and transepidermal water loss (TEWL), while the treatment significantly increased stratum corneum hydration compared with the control group [91]. Within this framework, there are conflicting scientific facts about the use of vinegar as a natural remedy for atopic dermatitis, but it could be a departure point for conducting deep experimental research comparing different types of fruit vinegars well known for their pleiotropic action.
Mastitis
Mastitis is a mammary gland disorder involving inflammation. Mastitis-causing agents can be classified into major and minor pathogens [92]. Chemical germicide agents used to treat mastitis have numerous side effects, including milk contamination [92]. The search for safe and effective natural agents constitutes the main objective of the new scientific trend of using natural products. An ethnoveterinary survey conducted in Turkey to catalog traditional knowledge of herbal medicinal use documented that numerous medicinal plants were used in treating mastitis and improving milk production, including Urtica dioica L. MK-105, Smilax excelsa L. MK-1459, Acer heldreichii subsp. trautvetteri (Medw.) A.E. Murray MK-1044, Prunus laurocerasus L. MK-1193, and Bellis perennis L. MK-1179 [93]. Fruit vinegar is a natural remedy with multifaceted properties that could be useful for treating mastitis. The examination of the ability of acetic acid on mastitis pathogens showed interesting results compared with other acids such as lactic, lauric, and caprylic acids [92]. Acetic acid is the main organic acid of vinegar that is scientifically proven to exhibit strong antimicrobial effects against pathogens with high-antibiotic resistance [94–96]. It has been noteworthy to be noted that the main microorganisms implicated in mastitis, including Escherichia coli, Streptococcus uberis, and Staphylococcus, were highly sensitive to the effects of fruit vinegar, as previously confirmed by numerous published reports [97, 98]. Further investigations are required to evaluate the impact of fruit vinegar on mastitis.
Asthma
Asthma is a chronic disease in which inflammation plays a central role. The symptoms of asthma include wheezing, cough, and short breath [99]. Bronchodilators and anti-inflammatory medication are the most conventional treatments prescribed to treat asthma [70]. However, long-term and high doses limit their use because of the considerable side effects that appear during or after treatment [100]. The search for safe and effective compounds has redirected the interest of the scientific community toward natural products as a promising source of active ingredients, with fewer or non-adverse effects, that have proved their efficacy for treating asthma [101]. The dramatic increase in the use of fermented food to treat asthma has been noted [102]. Fruit vinegar is one of the most popular fermented foods widely used in traditional medicine [31]. The consumption of vinegar attenuated several effects of toxic agents such as hypercaloric diet, nicotine, hydrogen peroxide, high-fat-diet, phenylhydrazine, and so on [8, 54, 56, 103]. In addition, the application of vinegar ameliorates different diseases in which the inflammatory process orchestrated their development, including atopic dermatitis, arthritis, oxidative stress, and colitis [77, 78, 90, 104, 105]. In particular, fruit vinegar was found to control the production of the inflammatory markers, boost immune response, and control the gut microbiota that plays a pivotal role in the pathophysiology of asthma [102]. Dietary therapies are the first strategy to counteract different human diseases such as asthma [106, 107]. Squill oxymel as a traditional formulation containing vinegar as an ingredient, is used to treat severe persistent asthma, and its consumption for 6 weeks showed a significant improvement in forced expiratory volume in the first second (FEV1), forced expiratory flow between 25% and 75% (MEF 25–75%), also it was found that the formulation improved symptoms, activity, and score using pre- and post-intervention George’s respiratory questionnaire (SGRQ) [107]. The remarked beneficial properties of Oxymel could be due to its ability to modulate inflammatory processes and cholinergic activities [107]. In fact, the fruit vinegar administration successfully triggered inflammatory mediators in different animal models and human patients [20, 53, 55, 56, 107]. Scientific experiment showed that treatment with oak wood vinegar sustained 24 days attenuated the increase IgE production in 2,4-dinitrochlorobenzene (DNCB)-induced contact dermatitis mice model [78]. Additionally, nipa vinegar successfully proved its ability to suppress the expression of inflammatory mediators such as NF-kB and iNOS, which induce the reduction of NO levels (Fig. 1). The production of the highest amounts of NO indirectly activates Th2 cells, which are implicated in asthma physiopathology [108]. A historical review of inhalation therapies for asthma mentioned the vapor of vinegar [109]. Vinegar administration can adjust the production, secretion, and gene expression of airway mucin [110]. To establish confirmative evidence on the beneficial effects of fruit vinegar in asthma treatment, further investigative studies are needed. This could be a keystone of new original research.
Arthritis
Arthritis is a type of disease in which a chronic inflammatory process is involved and is characterized by discomfort and joint pain. Recently, the nutritional approach for illness conditions remains interesting because of its beneficial properties. Therefore, intensive scientific experiments have been conducted to confirm and examine the efficacy of this approach [111]. The investigation of the effect of apple cider vinegar in adjuvant arthritic rats is initiated by Ross et al., who concluded that this product is ineffective in treating this disease in rats [104]. In contrast, recent scientific evidence examined the ability of an innovative formulation of the Pangolin scale processed with vinegar (PSP) to decrease the arthritic index and inflammatory cell infiltration in the ankle joints of rats intoxicated by complete Freund’s adjuvant [112]. Accordingly, PSP lowered the serum levels of inflammatory cytokines, including TNF-α and IL-1ß [112]. Plentiful scientific evidence supports the ability of fruit vinegar to attenuate inflammatory processes induced by different toxic agents. However, other investigations are needed to elucidate the anti-arthritic effect of fruit vinegar.
Acute pancreatitis
The pancreas controls glycemia levels and is the target of numerous agents that induce acute pancreatitis, including drugs, alcohol, pancreatic ductal obstruction, and endoscopic retrograde cholangiopancreatography [113]. Calcium plays a pivotal role in acute pancreatitis installation through its elevation in acinar cells, which induces inflammation and pro-cell death [113]. In addition, mitochondrial dysfunction is implicated in the development of acute pancreatitis [114, 115]. Therefore, the control of mitochondrial function, calcium signaling pathways, and inflammatory processes could be useful in improving acute pancreatitis. Fruit vinegar has been widely used throughout the ages by several civilizations to treat digestive disorders [2]. The phytochemical complexity of fruit vinegar makes it a promising candidate for alleviating and treating many ailments, including inflammation, oxidative stress, obesity, and diabetes [3, 6, 15, 78, 116]. Pretreatment with vinegar demonstrated its ability to control voltage-dependent anion channel 1 (VDAC1), inhibit oxidative stress, and prevent mitochondrial dysfunction [117]. Tetramethylpyrazine is one of the most interesting active ingredients of vinegar, and it has been implicated in the prevention of acute pancreatitis in an animal model by inhibiting of nuclear factor-kappa B (NF-ĸß) [118]. Control of NF-ĸß activation and production of pro-inflammatory markers constitute a target of the therapeutic approach to acute pancreatitis. A study conducted by Choi et al. found that vinegar improved pro-inflammatory markers such as NO, iNOS, TNF-α IL-6, and MCP-1, which are involved in the inflammatory response [56]. Furthermore, ligustrazine, an active ingredient of vinegar, has shown promising results in acute pancreatitis, promoting acinar cell apoptosis at the early stage and downregulation the p38 and Erk MAP pathways [119]. There is no report on the beneficial effect of the direct administration of fruit vinegar on acute pancreatitis. Within this framework, further studies are needed to explore the pharmacological properties of vinegar on pancreatitis.
Colitis
Fruit vinegar is a natural product with multifaceted beneficial properties. It has been described as an effective cure for numerous human diseases recommended by several traditional healers [31]. Colitis is a type of disease treated with vinegar, and its effect was confirmed by Shizuma et al. by testing the ability of Kurozu (Traditional Japanese black vinegar) to attenuate dextran sulfate sodium-induced colitis. The authors showed that the administration of this product to C57 black 6 mice for twelve days proved a protective effect against the deleterious effects of DSS-induced colitis, decreasing nitrotyrosine levels and attenuating inflammatory modifications in rectal tissues [105]. In addition, Kurozu can suppress colitis symptoms such as bloody feces and body weight loss [120]. Vinegar has proven its potential to prevent the upregulation of IL-1ß and IL-6 mRNA (Fig. 2) [121]. Several studies indicate that fruit vinegar controls the development of different intestinal flora, thereby avoiding microbe-derived toxic metabolites, which could enhance the development of metabolic disorders. Fruit vinegar can maintain the homeostasis between luminal antigens and the intestinal defense system because of its potential to relieve the epithelial barrier and increase the number of commensal lactic or acetic acid-producing bacteria [55, 116].
Fig. 2.
Impact of bioactive compounds of fruit vinegar on different organs (Created in biorender.com)
The gastrointestinal tract is the main target of numerous agents causing ROS overproduction, which is attributed to toxic agents, dietary ingredients, pathogenic bacteria, and their interaction with immune cells [122, 123]. Treatment with vinegar or acetic acid was shown to be effective against histopathological damage induced by DSS-destroying crypts, mononuclear cell infiltration, goblet cell loss, and mucosal damage in the colon [116]. Vinegar ability to suppress Th1 and Th17 responses and attenuate inflammatory cytokine expression could explain its positive impact on colitis [116].
Limitations and future recommendations
The physical, chemical, and microbiological changes that occur during the fruit fermentation process have a significant impact on the vinegar’s quality and determine the final product’s distinctive aroma and flavor. Fruit vinegar could serve as a target for a variety of uses due to its physicochemical properties, including as an ecological solvent, a treatment for inflammatory diseases, and a cure for neurological disorders, and more. The major problem in investigating how fruit vinegar functions in humans is to conduct clinical investigations. Studies on ethnopharmacology have revealed a huge number of traditional uses for fruit vinegar that vary according to civilization, culture, religion, and region. However, it is crucial to identify the precise mechanisms underlying fruit vinegar’s anti-inflammatory and immunomodulatory effects.
Conclusion
As research progressed, fruit vinegar became an interesting food ingredient due to its wide spectrum of active compounds, ultimately affecting various target tissues. Emerging evidence from experimental studies on the anti-inflammatory effect of fruit vinegar for health-promoting features throughout controlling intestinal microbiota and pro-inflammatory cytokine production. Thus, the chemical complexity of vinegar constitutes a framework for intestinal flora to produce numerous compounds such as SCFAs implicated in different biological properties.
Supplementary information
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Author contributions
Conceptualization and writing original draft-review: Driss OUSAAID; writing, review, and editing: Meryem BAKOUR, Hassan LAAROUSSI, Asmae EL GHOUIZI; supervision: Badiaa LYOUSI and Ilham EL ARABI.
Funding
No funding received.
Data Availability
The data used to support the findings of this study are included within the article.
Declarations
Ethical approval
Not applicable.
Conflict of interest
The authors confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
Footnotes
Publisher’s Note
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References
- 1.Solieri L, Giudici P. Vinegars of the World. In: Solieri L, Giudici P, editors. Vinegars of the World. Milano: Springer Milan; 2009. pp. 1–16. [Google Scholar]
- 2.Mazza S, Murooka T. Vinegar Through the Ages. In: Solieri L, Giudici P, editors. Vinegars of the World. Milano: Springer; 2009. pp. 17–39. [Google Scholar]
- 3.Xia T, Zhang Z, Zhao Y, Kang C, Zhang X, Tian Y, Yu J, Cao H, Wang M. The anti-diabetic activity of polyphenolsrich vinegar extract in mice via regulating gut microbiota and liver inflammation. Food Chem. 2022;393:133443. doi: 10.1016/j.foodchem.2022.133443. [DOI] [PubMed] [Google Scholar]
- 4.Tripathi S, Mazumder PM. Neuroprotective efficacy of apple cider vinegar on zinc-high fat diet-induced mono amine oxidase alteration in murine model of AD. J Am Coll Nutr. 2021;41(7):658–667. doi: 10.1080/07315724.2021.1948933. [DOI] [PubMed] [Google Scholar]
- 5.Xia T, Zhang B, Duan W, Li Y, Zhang J, Song J, et al. Hepatoprotective efficacy of Shanxi aged vinegar extract against oxidative damage in vitro and in vivo. J Funct Foods. 2019;60:103448. doi: 10.1016/j.jff.2019.103448. [DOI] [Google Scholar]
- 6.Tong C, Li X, Cai C, Shi X, Li W. Hepatoprotective and lipid-lowering effect of an apple vinegar beverage with oyster polysaccharides. Научные Труды Дальрыбвтуза. 2019;47:57–64. [Google Scholar]
- 7.Erdal B, Yıkmış S, Demirok NT, Bozgeyik E, Levent O. Effects of non-thermal treatment on Gilaburu vinegar (Viburnum opulus L.): polyphenols, amino acid, antimicrobial, and anticancer properties. Biology. 2022;11:926. doi: 10.3390/biology11060926. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ali Z, Ma H, Wali A, Ayim I, Sharif MN. Daily date vinegar consumption improves hyperlipidemia, β-carotenoid and inflammatory biomarkers in mildly hypercholesterolemic adults. J Herb Med. 2019;17–18:100265. doi: 10.1016/j.hermed.2019.100265. [DOI] [Google Scholar]
- 9.Naseem E, Shamim M, Khan NI. Cardioprotective effects of herbal mixture (ginger, garlic, lemon, apple cider vinegar & honey) in experimental animal models of hyperlipidemia. Int J Biol Res. 2016;4:28–33. [Google Scholar]
- 10.Hwa HS, Kwon M, Lee HY, Park YM, Shin D-Y, Choi JS, et al. Immunomodulatory effect of fermented vinegar on cyclophosphamide-induced immunosuppression model. J Food Nutr Res. 2021;9:469–476. doi: 10.12691/jfnr-9-9-3. [DOI] [Google Scholar]
- 11.Yim EJ, Jo SW, Kang HJ, Park SK, Yu KY, Jeong D-Y, et al. Protection against osteoporosis by Fermented Mulberry vinegar supplementation via inhibiting osteoclastic activity in ovariectomized rats and osteoclastic cells. Fermentation. 2022;8:211. doi: 10.3390/fermentation8050211. [DOI] [Google Scholar]
- 12.Meng H, Song J, Fan B, Li Y, Zhang J, Yu J, et al. Monascus vinegar alleviates high-fat-diet-induced inflammation in rats by regulating the NF-κB and PI3K/AKT/mTOR pathways. Food Sci Hum Wellness. 2022;11:943–953. doi: 10.1016/j.fshw.2022.03.024. [DOI] [Google Scholar]
- 13.Es-sbata I, Castro R, Durán-Guerrero E, Zouhair R, Astola A. Production of prickly pear (Opuntia ficus-indica) vinegar in submerged culture using acetobacter malorum and gluconobacter oxydans: study of volatile and polyphenolic composition. J Food Compos Anal. 2022;112:104699. doi: 10.1016/j.jfca.2022.104699. [DOI] [Google Scholar]
- 14.Özdemir N, Pashazadeh H, Zannou O, Koca I. Phytochemical content, and antioxidant activity, and volatile compounds associated with the aromatic property, of the vinegar produced from rosehip fruit (Rosa canina L) Lwt. 2022;154:112716. doi: 10.1016/j.lwt.2021.112716. [DOI] [Google Scholar]
- 15.Ousaaid D, Mechchate H, Laaroussi H, Hano C, Bakour M, El Ghouizi A, et al. Fruits vinegar: quality characteristics, phytochemistry, and functionality. Molecules. 2021;27:222. doi: 10.3390/molecules27010222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Ali Z, Li J, Zhang Y, Naeem N, Younas S, Javeed F. Dates (Phoenix Dactylifera) and date vinegar: preventive role against various Diseases and related in vivo mechanisms. Food Rev Intl. 2022;38:480–507. doi: 10.1080/87559129.2020.1735411. [DOI] [Google Scholar]
- 17.Mumtaz S, Ali S, Tahir HM, Kazmi SAR, Shakir HA, Mughal TA, et al. Aging and its treatment with vitamin C: a comprehensive mechanistic review. Mol Biol Rep. 2021;48:8141–8153. doi: 10.1007/s11033-021-06781-4. [DOI] [PubMed] [Google Scholar]
- 18.Maya-Cano DA, Arango-Varela S, Santa-Gonzalez GA. Phenolic compounds of blueberries (Vaccinium spp) as a protective strategy against skin cell damage induced by ROS: a review of antioxidant potential and antiproliferative capacity. Heliyon. 2021;7:e06297. doi: 10.1016/j.heliyon.2021.e06297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Ai L, Ren Y, Zhu M, Lu S, Qian Y, Chen Z, et al. Synbindin restrains proinflammatory macrophage activation against microbiota and mucosal inflammation during Colitis. Gut. 2021;70:2261–2272. doi: 10.1136/gutjnl-2020-321094. [DOI] [PubMed] [Google Scholar]
- 20.Meng H, Song J, Li Y, Li X, Li X, Gou J, et al. Monascus vinegar protects against liver inflammation in high-fat-diet rat by alleviating intestinal microbiota dysbiosis and enteritis. J Funct Foods. 2022;93:105078. doi: 10.1016/j.jff.2022.105078. [DOI] [Google Scholar]
- 21.Tovar CA, Lima KO, Alemán A, Montero MP, Gómez-Guillén MC. The effect of chitosan nanoparticles on the rheo-viscoelastic properties and lipid digestibility of oil/vinegar mixtures (vinaigrettes) J Funct Foods. 2022;93:105092. doi: 10.1016/j.jff.2022.105092. [DOI] [Google Scholar]
- 22.ibn Al-Hajjaj M, al-Husain A. Sahih Muslim. Juz VI: Dar Al-Jail, Beirut, Tt; 2007.
- 23.Coskun O. Separation techniques: Chromatography. North Clin Istanb. 2016;3:156–160. doi: 10.14744/nci.2016.32757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Budak NH, Kumbul Doguc D, Savas CM, Seydim AC, Kok Tas T, Ciris MI, et al. Effects of apple cider vinegars produced with different techniques on blood lipids in high-cholesterol-fed rats. J Agric Food Chem. 2011;59:6638–6644. doi: 10.1021/jf104912h. [DOI] [PubMed] [Google Scholar]
- 25.Ousaaid D, Laaroussi H, Bakour M, El Ghouizi A, Mechchate H, Es-safi I, et al. New insights into Phytochemical Content and antioxidant activities of Moroccan Fruit vinegars. Chemistry Africa. 2022 doi: 10.1007/s42250-022-00427-z. [DOI] [Google Scholar]
- 26.Chochevska M, Jančovska Seniceva E, Veličkovska SK, Naumova-Leţia G, Mirčeski V, Rocha JMF, et al. Electrochemical determination of antioxidant capacity of traditional homemade fruit vinegars produced with double spontaneous fermentation. Microorganisms. 2021;9:1946. doi: 10.3390/microorganisms9091946. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Antoniewicz J, Kochman J, Jakubczyk K, Janda-Milczarek K. The influence of time and storage conditions on the antioxidant potential and total phenolic content in homemade grape vinegars. Molecules. 2021;26:7616. doi: 10.3390/molecules26247616. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Ousaaid D, Ghouizi AE, Laaroussi H, Bakour M, Mechchate H, Es-safi I, et al. Anti-anemic effect of antioxidant-rich apple vinegar against phenylhydrazine-induced hemolytic anemia in rats. Life. 2022;12:239. doi: 10.3390/life12020239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Aykın E, Budak NH, Güzel-Seydim ZB. Bioactive components of mother vinegar. J Am Coll Nutr. 2015;34:80–89. doi: 10.1080/07315724.2014.896230. [DOI] [PubMed] [Google Scholar]
- 30.Ren M, Wang X, Tian C, Li X, Zhang B, Song X, et al. Characterization of organic acids and phenolic compounds of cereal vinegars and fruit vinegars in China. J Food Process Preserv. 2017;41:e12937. doi: 10.1111/jfpp.12937. [DOI] [Google Scholar]
- 31.Budak NH, Aykin E, Seydim AC, Greene AK, Guzel-Seydim ZB. Functional properties of vinegar. J Food Sci. 2014;79:R757–764. doi: 10.1111/1750-3841.12434. [DOI] [PubMed] [Google Scholar]
- 32.Luzón-Quintana LM, Castro R, Durán-Guerrero E. Biotechnological processes in fruit vinegar production. Foods. 2021;10:945. doi: 10.3390/foods10050945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Liu Q, Tang G-Y, Zhao C-N, Gan R-Y, Li H-B. Antioxidant activities, phenolic profiles, and organic acid contents of fruit vinegars. Antioxidants. 2019;8:78. doi: 10.3390/antiox8040078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Liu Z, Wang C, Chen H, Ren X, Li W, Xu N, et al. Effect of changing the melanoidins by decoction on the release of volatiles in Zhenjiang aromatic vinegar. Food Res Int. 2022;158:111453. doi: 10.1016/j.foodres.2022.111453. [DOI] [PubMed] [Google Scholar]
- 35.Tagliazucchi D, Verzelloni E, Conte A. Antioxidant properties of traditional balsamic vinegar and boiled must model systems. Eur Food Res Technol. 2008;227:835–843. doi: 10.1007/s00217-007-0794-6. [DOI] [Google Scholar]
- 36.Chen J-C, Chen Q-H, Guo Q, Ruan S, Ruan H, He G-Q, et al. Simultaneous determination of acetoin and tetramethylpyrazine in traditional vinegars by HPLC method. Food Chem. 2010;122:1247–1252. doi: 10.1016/j.foodchem.2010.03.072. [DOI] [Google Scholar]
- 37.Wu J, Zhao H, Du M, Song L, Xu X. Dispersive liquid–liquid microextraction for rapid and inexpensive determination of tetramethylpyrazine in vinegar. Food Chem. 2019;286:141–145. doi: 10.1016/j.foodchem.2019.01.159. [DOI] [PubMed] [Google Scholar]
- 38.Shahidi F, Peng H. Bioaccessibility and bioavailability of phenolic compounds. J Food Bioactives. 2018;4:11–68. doi: 10.31665/JFB.2018.4162. [DOI] [Google Scholar]
- 39.Angelino D, Cossu M, Marti A, Zanoletti M, Chiavaroli L, Brighenti F, et al. Bioaccessibility and bioavailability of phenolic compounds in bread: a review. Food Funct. 2017;8:2368–2393. doi: 10.1039/C7FO00574A. [DOI] [PubMed] [Google Scholar]
- 40.Bakir S, Toydemir G, Boyacioglu D, Beekwilder J, Capanoglu E. Fruit antioxidants during vinegar processing: changes in content and in vitro bio-accessibility. Int J Mol Sci. 2016;17:1658. doi: 10.3390/ijms17101658. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.McDougall GJ, Dobson P, Smith P, Blake A, Stewart D. Assessing potential bioavailability of Raspberry anthocyanins using an in vitro digestion system. J Agric Food Chem. 2005;53:5896–5904. doi: 10.1021/jf050131p. [DOI] [PubMed] [Google Scholar]
- 42.Toydemir G, Boyacioglu D, Capanoglu E, van der Meer IM, Tomassen MMM, Hall RD, et al. Investigating the transport dynamics of anthocyanins from unprocessed fruit and processed fruit juice from sour cherry (Prunus cerasus L.) across intestinal epithelial cells. J Agric Food Chem. 2013;61:11434–11441. doi: 10.1021/jf4032519. [DOI] [PubMed] [Google Scholar]
- 43.Gonthier M-P, Verny M-A, Besson C, Rémésy C, Scalbert A. Chlorogenic acid bioavailability largely depends on its metabolism by the gut microflora in rats. J Nutr. 2003;133:1853–1859. doi: 10.1093/jn/133.6.1853. [DOI] [PubMed] [Google Scholar]
- 44.Kishida K, Matsumoto H. Urinary excretion rate and bioavailability of chlorogenic acid, caffeic acid, p-coumaric acid, and ferulic acid in non-fasted rats maintained under physiological conditions. Heliyon. 2019;5:e02708. doi: 10.1016/j.heliyon.2019.e02708. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Quirós-Sauceda AE, Palafox-Carlos H, Sáyago-Ayerdi SG, Ayala-Zavala JF, Bello-Perez LA, Alvarez-Parrilla E, et al. Dietary fiber and phenolic compounds as functional ingredients: interaction and possible effect after ingestion. Food Funct. 2014;5:1063–1072. doi: 10.1039/C4FO00073K. [DOI] [PubMed] [Google Scholar]
- 46.Grgić J, Šelo G, Planinić M, Tišma M, Bucić-Kojić A. Role of the encapsulation in bioavailability of phenolic compounds. Antioxidants. 2020;9:923. doi: 10.3390/antiox9100923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Carbonell-Capella JM, Buniowska M, Barba FJ, Esteve MJ, Frígola A. Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables: a review. Compr Rev Food Sci Food Saf. 2014;13:155–171. doi: 10.1111/1541-4337.12049. [DOI] [PubMed] [Google Scholar]
- 48.Zhao Y-S, Eweys AS, Zhang J-Y, Zhu Y, Bai J, Darwesh OM, et al. Fermentation affects the antioxidant activity of plant-based food material through the release and production of bioactive components. Antioxidants. 2021;10:2004. doi: 10.3390/antiox10122004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Thilakarathna SH, Rupasinghe HPV. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients. 2013;5:3367–3387. doi: 10.3390/nu5093367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Nie J, Li Y, Xing J, Chao J, Qin X, Li Z. Comparison of two types of vinegar with different aging times by NMR-based metabolomic approach. J Food Biochem. 2019;43:e12835. doi: 10.1111/jfbc.12835. [DOI] [PubMed] [Google Scholar]
- 51.Al-Dalali S, Zheng F, Sun B, Chen F. Comparison of aroma profiles of traditional and modern Zhenjiang aromatic vinegars and their changes during the vinegar aging by SPME-GC-MS and GC-O. Food Anal Methods. 2019;12:544–557. doi: 10.1007/s12161-018-1385-9. [DOI] [Google Scholar]
- 52.Yagnik D, Ward M, Shah AJ. Antibacterial apple cider vinegar eradicates methicillin resistant Staphylococcus aureus and resistant Escherichia coli. Sci Rep. 2021;11:1–7. doi: 10.1038/s41598-020-78407-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Wakuda T, Azuma K, Saimoto H, Ifuku S, Morimoto M, Arifuku I, et al. Protective effects of galacturonic acid-rich vinegar brewed from Japanese pear in a dextran sodium sulfate-induced acute Colitis model. J Funct Foods. 2013;5:516–523. doi: 10.1016/j.jff.2012.10.010. [DOI] [Google Scholar]
- 54.Ousaaid D, Laaroussi H, Bakour M, El Ghouizi A, Aboulghazi A, Lyoussi B, El Arabi I. Beneficial effects of apple vinegar on hyperglycemia and hyperlipidemia in hypercaloric-fed rats. J Diabetes Res. 2020;2020:1–7. doi: 10.1155/2020/9284987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Beh BK, Mohamad NE, Yeap SK, Ky H, Boo SY, Chua JYH, et al. Anti-obesity and anti-inflammatory effects of synthetic acetic acid vinegar and Nipa vinegar on high-fat-diet-induced obese mice. Sci Rep. 2017;7:1–9. doi: 10.1038/s41598-017-06235-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Choi J-H, Park S-E, Yeo S-H, Kim S. Anti-inflammatory and cytotoxicity effects of Cudrania tricuspidata fruits vinegar in a co-culture system with RAW264. 7 macrophages and 3T3-L1 adipocytes. Foods. 2020;9:1232. doi: 10.3390/foods9091232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Xu L, He S, Yin P, Li D, Mei C, Yu X, et al. Punicalagin induces Nrf2 translocation and HO-1 expression via PI3K/Akt, protecting rat intestinal epithelial cells from oxidative stress. Int J Hyperth. 2016;32:465–473. doi: 10.3109/02656736.2016.1155762. [DOI] [PubMed] [Google Scholar]
- 58.Lischka J, Schanzer A, Hojreh A, Ba-Ssalamah A, de Gier C, Valent I, et al. Circulating microRNAs 34a, 122, and 192 are linked to obesity-associated inflammation and metabolic Disease in pediatric patients. Int J Obes. 2021;45:1763–1772. doi: 10.1038/s41366-021-00842-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, et al. Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol. 2017;44:94–102. doi: 10.1016/j.copbio.2016.11.010. [DOI] [PubMed] [Google Scholar]
- 60.Tamang JP, Shin D-H, Jung S-J, Chae S-W. Functional properties of microorganisms in fermented foods. Front Microbiol. 2016;7:578. doi: 10.3389/fmicb.2016.00578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Hashimoto M, Obara K, Ozono M, Furuyashiki M, Ikeda T, Suda Y, et al. Separation and characterization of the immunostimulatory components in unpolished rice black vinegar (kurozu) J Biosci Bioeng. 2013;116:688–696. doi: 10.1016/j.jbiosc.2013.05.029. [DOI] [PubMed] [Google Scholar]
- 62.Han K, Bose S, Wang J, Kim B-S, Kim MJ, Kim E-J, et al. Contrasting effects of fresh and fermented kimchi consumption on gut microbiota composition and gene expression related to metabolic syndrome in obese Korean women. Mol Nutr Food Res. 2015;59:1004–1008. doi: 10.1002/mnfr.201400780. [DOI] [PubMed] [Google Scholar]
- 63.Voreades N, Kozil A, Weir TL. Diet and the development of the human intestinal microbiome. Front Microbiol. 2014;5:5. doi: 10.3389/fmicb.2014.00494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci. 2013;110:9066–71. doi: 10.1073/pnas.1219451110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Sengun IY, Kilic G, Ozturk B. Screening physicochemical, microbiological and bioactive properties of fruit vinegars produced from various raw materials. Food Sci Biotechnol. 2020;29:401–408. doi: 10.1007/s10068-019-00678-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Xia T, Zhang B, Duan W, Zhang J, Wang M. Nutrients and bioactive components from vinegar: a fermented and functional food. J Funct Foods. 2020;64:103681. doi: 10.1016/j.jff.2019.103681. [DOI] [Google Scholar]
- 67.Dibner JJ, Buttin P. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J Appl Poult Res. 2002;11:453–463. doi: 10.1093/japr/11.4.453. [DOI] [Google Scholar]
- 68.Zare R, Abedian Kenari A, Yazdani Sadati M. Influence of dietary acetic acid, protexin (probiotic), and their combination on growth performance, intestinal microbiota, digestive enzymes, immunological parameters, and fatty acids composition in Siberian sturgeon (Acipenser baerii, Brandt, 1869) Aquacult Int. 2021;29:891–910. doi: 10.1007/s10499-021-00652-2. [DOI] [Google Scholar]
- 69.Dai D, Qiu K, Zhang H, Wu S, Han Y, Wu Y, Qi G, Wang J. Organic acids as alternatives for antibiotic growth promoters alter the intestinal structure and microbiota and improve the growth performance in Broilers. Fron Microbiol. 2021;11:1–14. doi: 10.3389/fmicb.2020.618144. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Jiang D, Kang A, Yao W, Lou J, Zhang Q, Bao B, et al. Euphorbia kansui fry-baked with vinegar modulates gut microbiota and reduces intestinal toxicity in rats. J Ethnopharmacol. 2018;226:26–35. doi: 10.1016/j.jep.2018.07.029. [DOI] [PubMed] [Google Scholar]
- 71.Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, De Los Reyes-gavilán CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185. doi: 10.3389/fmicb.2016.00185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and Colorectal cancer. Nat Rev Microbiol. 2014;12:661–672. doi: 10.1038/nrmicro3344. [DOI] [PubMed] [Google Scholar]
- 73.Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A Gnotobiotic Mouse Model demonstrates that dietary Fiber protects against colorectal tumorigenesis in a microbiota-and butyrate-dependent MannerFiber–Microbiota–butyrate Axis in Tumor suppression. Cancer Discov. 2014;4:1387–1397. doi: 10.1158/2159-8290.CD-14-0501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Den Besten G, Bleeker A, Gerding A, van Eunen K, Havinga R, van Dijk TH, et al. Short-chain fatty acids protect against high-fat diet–induced obesity via a PPARγ-dependent switch from lipogenesis to fat oxidation. Diabetes. 2015;64:2398–2408. doi: 10.2337/db14-1213. [DOI] [PubMed] [Google Scholar]
- 75.Jung T-H, Park JH, Jeon W-M, Han K-S. Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretion and MAPK signaling pathway. Nutr Res Pract. 2015;9:343–349. doi: 10.4162/nrp.2015.9.4.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Ho C-L, Lin C-Y, Ka S-M, Chen A, Tasi Y-L, Liu M-L, et al. Bamboo vinegar decreases inflammatory mediator expression and NLRP3 inflammasome activation by inhibiting reactive oxygen species generation and protein kinase C-α/δ activation. PLoS ONE. 2013;8:e75738. doi: 10.1371/journal.pone.0075738. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Xia T, Zhang J, Yao J, Zhang B, Duan W, Zhao C, et al. Shanxi aged vinegar protects against alcohol-induced liver injury via activating Nrf2-mediated antioxidant and inhibiting TLR4-induced inflammatory response. Nutrients. 2018;10:805. doi: 10.3390/nu10070805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Lee CS, Yi EH, Kim H-R, Huh S-R, Sung S-H, Chung M-H, et al. Anti-dermatitis effects of oak wood vinegar on the DNCB-induced contact hypersensitivity via STAT3 suppression. J Ethnopharmacol. 2011;135:747–753. doi: 10.1016/j.jep.2011.04.009. [DOI] [PubMed] [Google Scholar]
- 79.Dizon MP, Yu AM, Singh RK, Wan J, Chren M-M, Flohr C, et al. Systematic review of atopic dermatitis Disease definition in studies using routinely collected health data. Br J Dermatol. 2018;178:1280–1287. doi: 10.1111/bjd.16340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Bath-Hextall FJ, Birnie AJ, Ravenscroft JC, Williams HC. Interventions to reduce Staphylococcus aureus in the management of atopic eczema: an updated Cochrane review. Br J Dermatol. 2010;163:12–26. doi: 10.1111/j.1365-2133.2010.09743.x. [DOI] [PubMed] [Google Scholar]
- 81.Rippke F, Schreiner V, Doering T, Maibach HI. Stratum corneum pH in atopic dermatitis. Am J Clin Dermatol. 2004;5:217–223. doi: 10.2165/00128071-200405040-00002. [DOI] [PubMed] [Google Scholar]
- 82.Proksch E. pH in nature, humans and skin. J Dermatol. 2018;45:1044–1052. doi: 10.1111/1346-8138.14489. [DOI] [PubMed] [Google Scholar]
- 83.Luu LA, Flowers RH, Kellams AL, Zeichner S, Preston DC, Zlotoff BJ, et al. Apple cider vinegar soaks [0.5%] as a treatment for atopic dermatitis do not improve skin barrier integrity. Pediatr Dermatol. 2019;36:634–639. doi: 10.1111/pde.13888. [DOI] [PubMed] [Google Scholar]
- 84.Lim NR, Treister AD, Tesic V, Lee KC, Lio PA. A split body trial comparing dilute bleach vs. dilute apple cider vinegar compresses for atopic dermatitis in Chicago: a pilot study. J Dermatol Cosmetol. 2019;3:22–24. doi: 10.15406/jdc.2019.03.00109. [DOI] [Google Scholar]
- 85.Chopra R, Vakharia PP, Sacotte R, Silverberg JI. Efficacy of bleach baths in reducing severity of atopic dermatitis: a systematic review and meta-analysis. Ann Allergy Asthma Immunol. 2017;119:435–440. doi: 10.1016/j.anai.2017.08.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 86.Wong S, Ng TG, Baba R. Efficacy and safety of sodium hypochlorite (bleach) baths in patients with moderate to severe atopic dermatitis in Malaysia. J Dermatol. 2013;40:874–880. doi: 10.1111/1346-8138.12265. [DOI] [PubMed] [Google Scholar]
- 87.Sawada Y, Tong Y, Barangi M, Hata T, Williams MR, Nakatsuji T, et al. Dilute bleach baths used for treatment of atopic dermatitis are not antimicrobial in vitro. J Allergy Clin Immunol. 2019;143:1946–1948. doi: 10.1016/j.jaci.2019.01.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 88.Eriksson S, Van der Plas MJA, Mörgelin M, Sonesson A. Antibacterial and antibiofilm effects of sodium hypochlorite against Staphylococcus aureus isolates derived from patients with atopic dermatitis. Br J Dermatol. 2017;177:513–521. doi: 10.1111/bjd.15410. [DOI] [PubMed] [Google Scholar]
- 89.Ousaaid D, Laaroussi H, Bakour M, Ennaji H, Lyoussi B, El Arabi I. Antifungal and antibacterial activities of apple vinegar of different cultivars. Int J Microbiol. 2021;2021:1–6. doi: 10.1155/2021/6087671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 90.Luu LA, Flowers RH, Gao Y, Wu M, Gasperino S, Kellams AL, et al. Apple cider vinegar soaks do not alter the skin bacterial microbiome in atopic dermatitis. PLoS ONE. 2021;16:e0252272. doi: 10.1371/journal.pone.0252272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91.Lee NR, Lee H-J, Yoon NY, Kim D, Jung M, Choi EH. Application of topical acids improves atopic dermatitis in murine model by enhancement of skin barrier functions regardless of the origin of acids. Ann Dermatol. 2016;28:690–696. doi: 10.5021/ad.2016.28.6.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92.Pangprasit N, Srithanasuwan A, Suriyasathaporn W, Pikulkaew S, Bernard JK, Chaisri W. Antibacterial activities of acetic acid against major and minor pathogens isolated from mastitis in dairy cows. Pathogens. 2020;9:961. doi: 10.3390/pathogens9110961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93.Güler O, Polat R, Karaköse M, Çakılcıoğlu U, Akbulut S. An ethnoveterinary study on plants used for the treatment of livestock Diseases in the province of Giresun (Turkey) South Afr J Bot. 2021;142:53–62. doi: 10.1016/j.sajb.2021.06.003. [DOI] [Google Scholar]
- 94.Ousaaid D, Imtara H, Laaroussi H, Lyoussi B, El Arabi I. An investigation of Moroccan vinegars: Their physicochemical properties and antioxidant and antibacterial activities. J Food Qual. 2021;2021:1–8. doi: 10.1155/2021/6618444. [DOI] [Google Scholar]
- 95.Ikechukwu N, Oriki-Udezuka A. Antibacterial effect of vinegar produced from Garcina Kola and Artocarpus heterophyllus. Asian J Microbiol Biotechnol. 2021;12(2):48–60. [Google Scholar]
- 96.El-Sayed TS, Nour El-Deen MM, Rokaya ME, Sherif MM. Evaluation of the antibacterial effect of apple vinegar as a root canal irrigant using endovac irrigation system. Al-Azhar Dent J Girls. 2019;6:53–59. doi: 10.21608/adjg.2019.28400. [DOI] [Google Scholar]
- 97.Hindi NK. In vitro antibacterial activity of aquatic garlic extract, apple vinegar and apple vinegar-garlic extract combination. Am J Phytomedicine Clin Ther. 2013;1:42–51. [Google Scholar]
- 98.Entani E, Asai M, Tsujihata S, Tsukamoto Y, Ohta M. Antibacterial action of vinegar against food-borne pathogenic bacteria including Escherichia coli O157: H7. J Food Prot. 1998;61:953–959. doi: 10.4315/0362-028X-61.8.953. [DOI] [PubMed] [Google Scholar]
- 99.Hammad H, Lambrecht BN. The basic immunology of Asthma. Cell. 2021;184:1469–1485. doi: 10.1016/j.cell.2021.02.016. [DOI] [PubMed] [Google Scholar]
- 100.Agertoft L, Pedersen S. Effects of long-term treatment with an inhaled corticosteroid on growth and pulmonary function in asthmatic children. Respir Med. 1994;88:373–381. doi: 10.1016/0954-6111(94)90044-2. [DOI] [PubMed] [Google Scholar]
- 101.Amaral-Machado L, Oliveira WN, Moreira-Oliveira SS, Pereira DT, Alencar EN, Tsapis N, Egito ES. Use of natural products in asthma treatment. Evi-Based Complement Altern Med. 2020;2020:1–35. doi: 10.1155/2020/1021258. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 102.Dębińska A, Sozańska B. Fermented food in asthma and respiratory allergies—chance or failure? Nutrients. 2022;14:1420. doi: 10.3390/nu14071420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 103.Bouazza A, Bitam A, Amiali M, Bounihi A, Yargui L, Koceir EA. Effect of fruit vinegars on liver damage and oxidative stress in high-fat-fed rats. Pharm Biol. 2016;54:260–265. doi: 10.3109/13880209.2015.1031910. [DOI] [PubMed] [Google Scholar]
- 104.Ross CM, Poluhowich JJ. The effect of apple cider vinegar on adjuvant arthritic rats. Nutr Res. 1984;4:737–741. doi: 10.1016/S0271-5317(84)80049-4. [DOI] [Google Scholar]
- 105.Shizuma T, Ishiwata K, Nagano M, Mori H, Fukuyama N. Protective effects of Kurozu and Kurozu Moromimatsu on dextran sulfate sodium-induced experimental Colitis. Dig Dis Sci. 2011;56:1387–1392. doi: 10.1007/s10620-010-1432-x. [DOI] [PubMed] [Google Scholar]
- 106.Bussmann RW, Glenn A. Fighting pain: traditional Peruvian remedies for the treatment of asthma, rheumatism, arthritis and sore bones. IJTK. 2011;10(3):2011. [Google Scholar]
- 107.Nejatbakhsh F, Karegar-Borzi H, Amin G, Eslaminejad A, Hosseini M, Bozorgi M, et al. Squill Oxymel, a traditional formulation from Drimia maritima (L.) Stearn, as an add-on treatment in patients with moderate to severe persistent Asthma: a pilot, triple-blind, randomized clinical trial. J Ethnopharmacol. 2017;196:186–192. doi: 10.1016/j.jep.2016.12.032. [DOI] [PubMed] [Google Scholar]
- 108.Prado CM, Martinis MA, Tibério IS. Nitric oxide in asthma physiopathology. Int Sch Res Notices. 2011;2011:1–13. [Google Scholar]
- 109.Sanders M. Inhalation therapy: an historical review. Prim Care Respir J. 2007;16:71–81. doi: 10.3132/pcrj.2007.00017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 110.Kim H, Jung H-M, Kim S, Seo U-K. Effect of wood vinegar produced from Morus alba on HyperSecretion of Airway MUCUS. J Intern Korean Med. 2010;31:650–666. [Google Scholar]
- 111.García-Montero C, Fraile-Martínez O, Gómez-Lahoz AM, Pekarek L, Castellanos AJ, Noguerales-Fraguas F, et al. Nutritional components in Western diet versus mediterranean diet at the gut microbiota–immune system interplay. Implications for health and disease. Nutrients. 2021;13:699. doi: 10.3390/nu13020699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 112.Lv H, Li Z, Xie Z, Hu X, Li H, Sun J, et al. Innovated formulation of TCM pangolin scales to develop a nova therapy of rheumatoid arthritis. Biomed Pharmacother. 2020;126:109872. doi: 10.1016/j.biopha.2020.109872. [DOI] [PubMed] [Google Scholar]
- 113.Lee PJ, Papachristou GI. New insights into acute Pancreatitis. Nat Rev Gastroenterol Hepatol. 2019;16:479–496. doi: 10.1038/s41575-019-0158-2. [DOI] [PubMed] [Google Scholar]
- 114.Huang W, Booth DM, Cane MC, Chvanov M, Javed MA, Elliott VL, et al. Fatty acid ethyl ester synthase inhibition ameliorates ethanol-induced Ca2+-dependent mitochondrial dysfunction and acute Pancreatitis. Gut. 2014;63:1313–1324. doi: 10.1136/gutjnl-2012-304058. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 115.Trumbeckaite S, Kuliaviene I, Deduchovas O, Kincius M, Baniene R, Virketyte S, et al. Experimental acute Pancreatitis induces mitochondrial dysfunction in rat pancreas, kidney and lungs but not in liver. Pancreatology. 2013;13:216–224. doi: 10.1016/j.pan.2013.04.003. [DOI] [PubMed] [Google Scholar]
- 116.Shen F, Feng J, Wang X, Qi Z, Shi X, An Y, et al. Vinegar treatment prevents the development of murine experimental Colitis via inhibition of inflammation and apoptosis. J Agric Food Chem. 2016;64:1111–1121. doi: 10.1021/acs.jafc.5b05415. [DOI] [PubMed] [Google Scholar]
- 117.He H, Wang L, Qiao Y, Zhou Q, Yang B, Yin L, He M. Vinegar/Tetramethylpyrazine induces Nutritional Preconditioning protecting the myocardium mediated by VDAC1. Oxid Med Cell Longev. 2021;2021:1–17. doi: 10.1155/2021/6670088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 118.Chen L, Chen Y, Yun H, Jianli Z. Tetramethylpyrazine (TMP) protects rats against acute Pancreatitis through NF-κB pathway. Bioengineered. 2019;10:172–181. doi: 10.1080/21655979.2019.1613103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 119.Chen J, Chen J, Wang X, Wang C, Cao W, Zhao Y, et al. Ligustrazine alleviates acute Pancreatitis by accelerating acinar cell apoptosis at early phase via the suppression of p38 and Erk MAPK pathways. Biomed Pharmacother. 2016;82:1–7. doi: 10.1016/j.biopha.2016.04.048. [DOI] [PubMed] [Google Scholar]
- 120.Shizuma T. Anti-colitis effects of brown rice reported by experimental studies. J Rice Res. 2014;2:2. doi: 10.4172/jrr.1000127. [DOI] [Google Scholar]
- 121.Urtasun R, Díaz-Gómez J, Araña M, Pajares MJ, Oneca M, Torre P, et al. A combination of apple vinegar drink with Bacillus coagulans ameliorates high fat diet-induced body weight gain, insulin resistance and hepatic steatosis. Nutrients. 2020;12:2504. doi: 10.3390/nu12092504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 122.Thompson-Chagoyán OC, Maldonado J, Gil A. Aetiology of inflammatory bowel Disease (IBD): role of intestinal microbiota and gut-associated lymphoid tissue immune response. Clin Nutr. 2005;24:339–352. doi: 10.1016/j.clnu.2005.02.009. [DOI] [PubMed] [Google Scholar]
- 123.Rezaie A, Parker RD, Abdollahi M. Oxidative stress and pathogenesis of inflammatory bowel Disease: an epiphenomenon or the cause? Dig Dis Sci. 2007;52:2015–2021. doi: 10.1007/s10620-006-9622-2. [DOI] [PubMed] [Google Scholar]
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Data Availability Statement
The data used to support the findings of this study are included within the article.



