The inhibitory effects of plant additives on biogenic amine formation in fermented foods – a review

Abstract

Fermented food has unique properties and high nutritional value, and thus, should constitute a basic element of a balanced and health-promoting diet. However, it can accumulate considerable amount of biogenic amines (BAs), which ingested in excess can lead to adverse health effects. The application of plant-derived additives represents a promising strategy to ensure safety or enhance the functional and organoleptic properties of fermented food. This review summarizes currently available data on the application of plant-origin additives with the aim to reduce BA content in fermented products. The importance of ensuring fermented food safety has been highlighted considering the growing evidence of beneficial effects resulting from the consumption of this type of food, as well as the increasing number of individuals sensitive to BAs. The examined plant-origin additives reduced the BA concentration to varying degrees, and their efficacy depended on the type of additive, matrix, autochthonous, and inoculated microorganisms, as well as the manufacturing conditions. The main mechanisms of action include antimicrobial effects and the inhibition of microbial decarboxylases. Further research on the optimization of bioactive substances extraction, standardization of their chemical composition, and development of detailed procedures for its use in fermented products manufacturing are needed.

Graphical Abstract

Keywords:

• Biogenic amines
• plant extracts
• fermented food
• bioactive compounds
• antimicrobial effect
• human health

Introduction

According to the International Scientific Association for Probiotics and Prebiotics (ISAPP), the term “fermented foods and beverages” refers to “foods made through desired microbial growth and enzymatic conversions of food components” (Marco et al. 2021, 197). Because of the above, products in which development spoilage microorganisms were involved, should not be defined as “fermented”. Products that i) arise as a result of the fermentation process but do not contain viable microorganisms when consumed, such as bread, beer, wine, soy sauce, vinegar, and cheese, which are classified as “foods made by fermentation”, as well as ii) contain viable microorganisms, for example, yoghurt, kefir, non-heated fermented vegetables, belonging to the “contains live and active cultures” category, are included in the fermented food group (Marco et al. 2021). Several beneficial effects have been observed because of the enrichment of diets with either plant- or animal-origin fermented food (Das et al. 2020). The presence of compounds such as vitamins (B₂, B₉, B₁₂, and K), γ-aminobutyric acid (GABA), conjugated linoleic acids (CLA), exopolysaccharides, sphingolipids, bacteriocins, and bioactive peptides produced during the fermentation process is involved in this positive function (Chaudhary et al. 2021; Şanlier, Gökcen, and Sezgin 2019). Fermented food consumption can favorably alter the community and function of microorganisms (Kim and Park 2018; Nielsen et al. 2018; Taylor et al. 2020; Wastyk et al. 2021). Although fermented food consumption is highly recommended because of its multiple health-promoting effects, it can threaten the well-being of consumers with significant concentrations of biogenic amines (BAs) (Fong et al. 2020; Mah et al. 2019; Świder et al. 2020). These basic low-molecular-weight compounds are metabolized mainly by amine oxidase (AO) enzymes in the human body (Omer et al. 2021) but they can lead to adverse health effects when ingested in excess (Ladero et al. 2010) (Figure 1). Consumers suffering from histamine intolerance or being treated with specific medications, such as amino oxidase inhibitors are of particular concern because their BA metabolism is impaired (Comas-Basté et al. 2020; EFSA 2011). In 2011, the European Food Safety Authority (EFSA) released a scientific statement concerning the safety of fermented products with regard to BA occurrence, underlining the importance of further research on the limitations of these compounds in fermented foods (EFSA 2011). Thermal processing, which is widely employ in the food industry is not applicable for the purpose of BA control, because of the thermostability of these compounds (Alvarez and Moreno-Arribas 2014). Methods such as the application of not able to produce BAs or BA-degrading starter cultures have frequently been reported (Lee et al. 2021; Li et al. 2018; Zhang et al. 2022). Most of these methods resulted in a successful reduction of some BAs; however, the outcome differed between the tested microorganisms, indicating that decarboxylation and amino oxidation activities are strain-specific (Li and Lu 2020; Li et al. 2021). Moreover, some strains can either produce or degrade BAs (Tittarelli et al. 2019). Thus, individual strains must be thoroughly examined before being used as an inoculum. Researchers have pointed out food additives as a promising strategy to limit BA accumulation during fermentation. Substances such as nicotinic acid and glycine have been successfully used in Baechu kimchi fermentation (Jin et al. 2022). Phenolic acids (Zhang et al. 2018), polyphenols (Lee et al. 2018), plant/spices extracts (Jia et al. 2020; Jin et al. 2022; Lee et al. 2018; Mah, Kim, and Hwang 2009; Zhou et al. 2016), and seasonings (Majcherczyk and Surówka 2019) also showed a positive outcome regarding the reduction of BA content. Bioactive substances originating from plants, such as phenolic or nitrogen compounds, alkaloids, terpenes, polysaccharides, and pigments, can affect the profile and abundance of intestinal microorganisms and support homeostatic equilibrium (Luo et al. 2021; van der Merwe 2021). Thus, except for the limitation of BAs, enriching functional food with plant extracts represents a promising strategy for promoting the proper functioning of intestinal microorganisms, and consequently, other parts of the organism through gut-other organ axes (Ahlawat, Sharma, and Asha 2021; Barrio, Arias-Sánchez, and Martín-Monzón 2022). Furthermore, it can impart desirable flavor and is applicable either under industrial or household conditions.

Figure 1. Main microbial BA formation pathways in fermented food and fate of ingested BAs in human gastrointestinal tract. Abbreviations: TDC – tyrosine decarboxylase, LDC – lysine decarboxylase, HDC – histidine decarboxylase, ODC – ornithine decarboxylase, ADC – arginine decarboxylase, ADI – arginine deiminase, ARG – arginase, AGM – agmatinase, AgDI – agmatine deiminase. Prepared based on Benkerroum 2016; Erdag, Merhan, and Yildiz 2018; Ladero et al. 2010. Created with BioRender.com.

Considering the above, the purpose of this review was to provide insights into the currently available data on attempts to reduce BAs in fermented products through the application of plant-origin food additives. The effectiveness of the substances used in particular forms and concentrations in both plant- and animal-origin matrices was summarized, and their putative mechanisms of action were identified. The importance of providing safe fermented foods in terms of BA content has been emphasized from the viewpoint of human well-being, given the growing evidence for health-promoting features of fermented foods and the increasing number of consumers who are sensitive to BAs. Finally, future perspectives regarding plant-origin additive applications to fermented foods are put forward. To the best of our knowledge, this is the first review on the limitations of BAs in fermented products using plant-origin food additives.

Lactic acid bacteria (LAB) – their role in fermentation process and involvement in BA production

LAB are among the most important and commonly used microorganisms in the food-manufacturing industry. It consists of Gram-positive cocci or rods, and its main characteristics include its ability to convert carbohydrates into lactic acid during fermentation (Fessard and Remize 2017). Furthermore, compounds such as acetic acid, ethanol, bacteriocins, exopolysaccharides, carbon dioxide, vitamins, enzymes, and aromatic compounds represent other LAB metabolites, that determine the nutritional and sensory properties of the fermented products (de Souza, de Oliveira, and de Oliveira 2023; Leroy and De Vuyst 2004). Some of these can inhibit food-borne pathogens and spoilage microorganisms, consequently enhancing the safety and prolonging the shelf-life of food (de Souza, de Oliveira, and de Oliveira 2023; Tabanelli et al. 2014; Zhou et al. 2014). Considering their widespread natural occurrence in food, long-term applications, and rare involvement in diseases, most of LAB are generally recognized as safe (GRAS) (Bintsis 2018; Ghanbari et al. 2013). Based on the LAB community, two main stages of food fermentation have been distinguished. Leuconostoc and Weissella prevailed during the initial heterofermentation phase and produced both lactic and acetic acids. The successive homofermentation step, in which lactic acid is produced almost exclusively, is dominated by more acid-tolerant species such as Lactiplantibacillus plantarum, Levilactobacillus brevis, Latilactobacillus curvatus, and Lactobacillus sakei (Peñas et al. 2010; Wouters et al. 2013). Traditional and household manufacturing of fermented food is based on spontaneous processes in which native microorganisms present in the raw material are involved. Large-scale industrial production requires the use of well-examined starter strains that guarantee control over the process and standardization of the final product (Leroy and De Vuyst 2004).

Some authors have suggested that nonstarter lactic acid bacteria (NSLAB) exhibit different metabolic activities compared to industrial strains, that is, they produce more enzymes that convert amino acids and thus are of particular importance in the development of flavor. Therefore, isolation and characterization of wild-type strains from fermented foods, with the aim of applying them as starter cultures, represents a desirable measure in terms of the retention of product characteristics (Leroy and De Vuyst 2004; Sánchez et al. 2010). However, each strain intended to be used to initiate fermentation should be thoroughly tested for its ability to produce BAs, which are also products of amino acid metabolism (EFSA 2011). BAs are formed in the microbial cytoplasm mainly through the decarboxylation of the corresponding free amino acid (FAA) precursors. Tyrosine, phenylalanine, tryptophan, lysine, histidine, and arginine are the direct precursors of tyramine, phenylethylamine, tryptamine, cadaverine, histamine, and agmatine, respectively. In addition to its direct production from ornithine, putrescine can also be produced from glutamine, arginine, or agmatine. The agmatinase and agmatine deiminase pathways are two possible routes for the direct production of putrescine from agmatine. Indirect production from arginine involves the arginine deiminase or arginase pathway. Further transformation of putrescine into polyamines is catalyzed by spermidine and spermine synthase enzymes (Benkerroum 2016). Figure 1 depicts the reactions described above and figuratively refers to food safety indicating main mechanism of BA metabolism in human.

The regulation of oxidative and osmotic stresses, as well as the provision of metabolic energy and tolerance to acidic environments, are the main triggers of BA production by microbial cells (Benkerroum 2016). L. plantarum strains isolated from naturally fermented pickles produce up to 298, 994, 668, and 1332 mg/L of cadaverine, putrescine, histamine, and total BAs, respectively, when cultured in a medium supplemented with lysine, ornithine, and histidine (Alan, Topalcengiz, and Dığrak 2018). Considering that the authors examined neither the indirect production of putrescine from arginine nor other BA-formation abilities, that is the production of tyramine from tyrosine, it can be presumed that the final concentration of total BAs produced by the tested isolates can reach even higher values. On the other hand, among the 54 wild lactobacilli and pediococci biotypes isolated from Mountain Cheese, only 11 were BA producers. Five biotypes belonging to Pediococcus pentosaceus, two belonging to Lacticaseibacillus paracasei, and one belonging to Lentilactobacillus hilgardii could form tyramine, whereas three Lentilactobacillus parabuchneri biotypes synthesized histamine. None of the tested bacteria exhibited the ability to produce putrescine or cadaverine (Carafa et al. 2015). It has been demonstrated that products obtained through spontaneous fermentation can accumulate high concentrations of BA owing to the activity of autochthonous BA-positive microorganisms, and the application of an appropriate dose of BA-negative starter cultures can significantly reduce the content of these compounds (Gardini et al. 2016; Świder et al. 2023).

Fermented food consumption – implications for human health

Even though fermented foods represent an important part of numerous traditional diets (Aslam et al. 2020), the available consumption data are scarce and there is a need to complete the information regarding this subject matter (EFSA 2011). It has been estimated that more than 5,000 different types of fermented foods and beverages is manufactured and consumed throughout the world (Tamang, Watanabe, and Holzapfel 2016). According to assessment made by Campbell-Platt (1994) these products contribute to ca. one-third of the human diet. However, considering existing Western diet patterns on the one hand, and the growing health conscious of the consumers combined with facilitate access to different foods from all over the world on the other, today’s data on the consumption of fermented products can vary widely from almost 30 years old estimations. Recent results from The Netherlands indicate that fermented foods constitute approx. 16–18% of the adult Dutch diet, and subsequent 9–14% of consumed meals contain fermented ingredients (Li et al. 2020). One of the useful tools for searching the food consumption data regarding European countries is the EFSA Comprehensive European Food Consumption Database (EFSA 2022). It gathers information on the consumption of over 2,500 food groups, including fermented products. For example, according to the available surveys’ results the mean ingestion of fermented vegetables by adult consumers ranged from 6.00 (United Kingdom 2000) to 98.64 (Hungary 2018) g/day in 19 out of 27 countries included in the database. The current value of the fermented foods and beverages market equal USD 1.83 trillion and based on some statistical analysis it will continue to grow within the next five years (Fermented Foods and Beverages Market Size & Share Analysis – Growth Trends & Forecasts 2023–2028), what prove increasing demand for this type of food. Despite being significant part of a human diet, fermented products are still mostly override in nutritional guidelines (Bell, Ferrão, and Fernandes 2017).

The relationship between health and diet remains the subject of several studies worldwide. There is growing evidence for the anti-inflammatory properties of fermented foods. Kim and Park (2018) investigated the effects of kimchi consumption on selected health parameters. One treatment group consumed standard, whereas the other a functional product, made with organic Chinese cabbage, enriched with plant additives (mustard leaf, Chinese pepper, pear, shiitake mushrooms, sea tangle juice, mistletoe extract), and L. plantarum PNU starter culture. Beneficial effects, such as a significant decline in low-density lipoprotein (LDL) and an increase in high-density lipoprotein (HDL) cholesterol level, were observed in both groups. Additionally, in individuals consuming functional kimchi, there was a significant decrease in triglyceride, total cholesterol, and interleukin (IL)-6 levels (Kim and Park 2018). Meta-analysis of randomized control trials, including 26 studies, revealed that ingestion of fermented food can significantly reduce the levels of one of the inflammatory biomarkers, tumor necrosis factor (TNF)-α. The effects on the remaining investigated inflammation indicators, C-reactive protein and (IL)-6, were not demonstrated (SaeidiFard, Djafarian, and Shab-Bidar 2020). Increased gut microbiota diversity, as well as a decrease in 19 of 93 examined cytokines, chemokines, and other inflammatory serum proteins, including (IL)-6, levels were observed in individuals consuming fermented food over a 10-week intervention. Interestingly, the observed effects were not dependent on the amount of fermented food ingested or on body mass index (BMI). Additionally, such promising outcomes resulting from fermented food intake were not observed in high-fiber consumers (Wastyk et al. 2021). The anti-inflammatory properties of fermented products are summarized in an article by Kocot and Wróblewska (2021). Ingestion of fermented dairy products can support the prevention of development and enhance the treatment efficacy in patients with type 2 diabetes (Awwad et al. 2022; Teo et al. 2022). The presence of microorganisms and/or bioactive microbial metabolites produced during the fermentation process is the main factor that contributes to the potential anti-aging effects resulting from fermented food consumption (Das et al. 2020). Multiple studies have reported the anti-cancer properties of fermented products (Tasdemir and Sanlier 2020).

Gut microbiota vs. fermented food

In addition to regulatory effects on the digestive, nervous, and immune systems, and involvement in the metabolism and catabolism of consumed food ingredients, gut microbiota promotes the wellbeing of the human host through the inactivation of free radicals (Luo et al. 2021). Consumption of kimchi over 4 wk resulted in a change in the gut microbiota profile. The relative abundance of members of Clostridium sp. and species belonging to Escherichia and Shigella genera decreased, whereas Faecalibacterium, Roseburia, and Phasolactobacterium, which are involved in short chain fatty acid (SCFA) production, increased. Additionally, in individuals consuming functional kimchi, an increase in probiotic Bifidobacterium adolescentis was observed (Kim and Park 2018). In another study, patients with irritable bowel syndrome (IBS) were fed with pasteurized or non-pasteurized sauerkraut in a randomized trial. Gastrointestinal symptoms were mitigated, and the gut microbiota profile was altered in both groups. Although LAB occurred significantly more frequently in fecal samples of individuals consuming non-pasteurized sauerkraut, the results indicated that the presence of viable cells did not improve the condition of patients. The authors indicated the prebiotic substances available in the fermented products tested and secondary, high-temperature resistant metabolites produced by microorganisms, as putatively key beneficial factors (Nielsen et al. 2018). Analysis of the data acquired by the American Gut Project revealed that, except for differences in intestinal microbiota composition, consumers and non-consumers of fermented food were distinguished by CLA abundance. Higher levels of this compound in fecal samples of fermented food consumers putatively stem from endogenous or microbial production (Taylor et al. 2020).

The gut-brain relation represents an important part of nutritional psychiatry, as nutrition is one of the crucial factors affecting gut microbiota community (Oriach et al. 2016; van der Merwe 2021). Researchers have suggested that the consumption of fermented food, which is part of traditional dietary patterns, is particularly significant regarding the mental condition of human beings (Aslam et al. 2020; Selhub, Logan, and Bested 2014). The inclusion of fermented food in the dietary treatment of patients with anorexia nervosa (AN) was considered. Although there is a lack of unequivocal data proving the efficiency of such a strategy, further examination is important because recent research suggests that the gut microbiota is involved in the development of this eating disorder, and thus, dietary modulation of intestinal microorganisms can contribute to the improvement of the condition of patients with AN (Rocks et al. 2021). The connections between intestinal microorganisms and mental health remain a topic of debate (Barrio, Arias-Sánchez, and Martín-Monzón 2022; Kelly et al. 2016). It has been thoroughly supported that fecal microbiota transplantation from depressed patients to germ-free rats can trigger animal-recipient behaviors and physiological changes that co-occur with depression (Kelly et al. 2016). A review of recently published articles concerning the relationship between gut dysbiosis and brain-associated diseases indicated that probiotics and dietary fiber can positively affect cognitive functions as well as cortisol response (Barrio, Arias-Sánchez, and Martín-Monzón 2022). Similar conclusions were drawn by Casertano, Fogliano, and Ercolini (2022). In contrast, according to a meta-analysis based on 22 randomized control trials, the application of probiotics, prebiotics, and fermented food had no significant effect on cognitive functions. Statistical analysis of the pooled results indicated a lack of utility of such interventions, although 14 of the 22 trials included studies individually demonstrating a significant outcome. The authors indicated that the limited number of studies and lack of homogeneity of the methodology used may have contributed to the conclusions; thus, further studies are required (Marx et al. 2020).

Limitations in benefiting from the consumption of fermented food in the context of the presence of BAs

Several studies have indicated the potential positive effects of fermented food consumption on the psychological aspects of human well-being (Casertano, Fogliano, and Ercolini 2022). However, individuals with mental disorders are frequently treated with monoamine oxidase inhibitors (MAOIs); thus, they are particularly sensitive to BAs present in fermented products (EFSA 2011). Monoamine oxidases (MAOs) are enzymes involved in the regulation of amine neurotransmitter levels; therefore, they are an object of action of pharmacological substances used in the treatment of depression and Parkinson’s disease (Vianello, Repič, and Mavri 2012). Data from 1990–2016 indicate that depression is one of the five main global components of the years lived with disability (YLD) indicator, and the number of deaths and disabilities arising from Parkinson’s disease is growing the fastest among patients with neurological disorders, further indicating the broad scale of the problem (Schiess et al. 2022; Vos et al. 2017). According to the EFSA report, the no observed adverse effect level (NOAEL) of dietary tyramine in patients medicated with third-generation MAOI drugs is 12-fold lower than that in healthy individuals, whereas in cases of classical MAOI drugs, it is 100-fold lower (50 mg and 6 mg per person per meal, respectively) (EFSA 2011). These amounts can be easily ingested through available fermented products. Some widely used medicaments, for example antihypertensive and antibiotic, contain active substances that inhibits diamine oxidase (DAO) enzymes (Comas-Basté et al. 2020). Patients treated with such pharmaceuticals are threatened with higher risk of adverse health effects occurrence after ingestion of BAs. Another group that cannot fully benefit from the nutritiousness and health-promoting effects of fermented products in individuals with histamine intolerance (Comas-Basté et al. 2020). The diets of these individuals must be carefully composed to consider histamine as well as other amines, such as putrescine or spermidine, which can be metabolized by the same enzyme, that is DAO. Manufacturing fermented food with significantly low concentrations or lack of BAs is especially challenging, as fresh fruits and vegetables contain BAs (Sánchez-Pérez et al. 2018). Thus, the application of BA-degrading microorganisms alone or in combination with other methods appears to be an inevitable method to obtain safe fermented products. However, the levels of histamine and other BAs intake that trigger symptoms vary widely between individuals (Comas-Basté et al. 2020; Van den Eynde, Gillman, and Blackwell 2022) and a partial reduction of their content, which can be gained through plant additive application, may enable safer consumption of the product by sensitive individuals.

To date, little is known about the effects of the ingestion of fermented products other than dairy (Marco et al. 2021). Most researchers unanimously underlined that the health benefits resulting from fermented food consumption require further investigation, and human studies are required (Awwad et al. 2022; Das et al. 2020; Marco et al. 2021; Tasdemir and Sanlier 2020).

Bioactive compounds – superiority of fermented over non-fermented food

The health-promoting effects of fermented food originate mainly from the presence of beneficial microorganisms and/or bioactive compounds produced by microorganisms during fermentation (Das et al. 2020). GABA can enhance health maintenance due to diverse beneficial effects (Sahab et al. 2020). A report by Gan et al. (2017) revealed that fermented edible seeds contain from several to several dozen times more GABA than nonfermented samples. Bioactive peptides are another factor contributing to the health-promoting properties of fermented products. Antioxidative, antihypertensive, immunomodulatory, and cholesterol-lowering activities are among its main assets (Chaudhary et al. 2021). Strains exhibiting beneficial features have frequently been isolated from fermented products. Dextran produced by Pediococcus pentosaceus CRAG3, derived from fermented cucumbers, showed anti-cancer potential. The polymer inhibited the viability of cervical and colorectal cancer cells in an in vitro study (Shukla and Goyal 2013). Similar properties against colorectal cancer were exhibited by a soybean extract fermented with L. plantarum DGK-17 originating from kimchi (Khan and Kang 2017). The immunomodulatory, anti-inflammatory, antiallergic, cholesterol-lowering, weight loss, antioxidative, mental health, and gut function-enhancing effects of L. plantarum strains originating from fermented food have been summarized in a review by Garcia-Gonzalez et al. (2021). The quantity and profile of compounds produced during fermentation can vary among members of the same family or genus (Xu et al. 2021). Thus, thorough examination of individual strains should be performed to elucidate the potential health effects of fermented food matrices, as well as to gain insight into the possible applications of beneficial microorganisms.

Occurrence and toxicity of BAs in fermented foods

Amines produced de novo in plants or animals, also referred to as “endogenous amines”, are responsible for multiple physiological functions. In humans, these compounds are involved in the regulation of body temperature, secretion of gastric acids, immunological responses, gene expression, and growth and differentiation of cells. They also act as neurotransmitters and modulate brain activity regarding cognitive functions (Ladero et al. 2010). Although essential to life, the excessive ingestion of BAs in food can lead to adverse effects. The consumption of products containing high concentrations of histamine can trigger symptoms in the nervous, digestive, circulatory, and respiratory systems, as well as skin reactions, such as redness, rash, or urticaria (del Rio et al. 2017; Ladero et al. 2010). Histamine poisoning is also commonly referred to as “histamine fish poisoning” or “scombroid syndrome”, because it most often results from the consumption of fish, particularly members of the mackerel family (Scombridae) or fish products (del Rio et al. 2017; Velut et al. 2019). Although histamine is the only BA whose levels in some food products are legislatively limited, the results of in vitro studies indicate that it can be less toxic than tyramine (Linares et al. 2016). Symptoms of excessive tyramine intake include headache, migraines, vomiting, and neurological, blood pressure and respiratory disorders, which are referred to as the “cheese reaction” (del Rio et al. 2017; Gao et al. 2023; Ladero et al. 2010). Additionally, histamine and tyramine exhibit synergistic cytotoxic effects at concentrations found in food (del Rio et al. 2017). In severe cases, BA poisoning may lead to a sudden increase in blood pressure above 180/120 mm Hg, the so-called hypertensive crisis, which in turn may damage the organs of the cardiovascular or nervous system (Ladero et al. 2010). The literature has repeatedly emphasized the enhancing effect of putrescine and cadaverine on the toxicity of histamine, mainly due to the interaction of these BAs with the DAO enzyme involved in the metabolism of diamines (Ruiz-Capillas and Herrero 2019). Cytotoxicity studies of HT29 intestinal adenocarcinoma cells showed that putrescine and cadaverine at concentrations found in food can induce cell necrosis, with two-fold lower NOAEL and LOAEL (lowest observed adverse effect level) values for cadaverine (5 and 10 mM for putrescine, and 2.5 and 5 mM for cadaverine, respectively), and the cytotoxicity of these diamines is lower than that of tyramine and histamine (del Rio et al. 2019). Tryptamine and ß-phenylethylamine also exhibit cytotoxic effects through the induction of apoptosis and cell necrosis, respectively, and enhance histamine toxicity by inhibiting the DAO (tryptamine and ß-phenylethylamine) and histamine N-methyltransferase (HNMT; only ß-phenylethylamine) enzymes. Owing to their vasoconstrictive effects, tryptamine and ß-phenylethylamine can increase blood pressure and trigger vomiting, sweating, and headaches (del Rio et al. 2020). Another risk associated with BAs is their involvement in the formation of carcinogenic N-nitroso compounds (Fong, El-Nezami, and Sze 2021; Fong et al. 2020). The reaction of putrescine or spermidine with nitrous acid results in the formation of N-nitrosopyrrolidines (Kalač 2014). Polyamines (spermine and spermidine) can damage the retinal pigment epithelial cells, with spermine exhibiting a stronger effect (Kaneko et al. 2007). Despite numerous positive effects of agmatine, such as improvement of cognitive functions or regulation of the epithelial cell growth during wounds healing, excessive intake of this BA can provoke gastrointestinal symptoms, such as diarrhea and nausea (Gümrü, Şahin, and Aricioğlu 2013; Khémesse et al. 2023). As a precursor of putrescine, it also regulates polyamine levels (Khémesse et al. 2023). Susceptibility to BA intoxication differs among individuals and depends on the effectiveness of the detoxification system and whether a person is treated with MAOI/DAOI drugs. Alcohol consumption can increase the vulnerability to high doses of BAs (Comas-Basté et al. 2020).

Food fermentation aids in the formation of high concentrations of BAs because of the availability of proteins that can be converted into BA precursors, namely free amino acids (FAAs), the presence of microorganisms producing BAs, and hospitable conditions for their growth and activity (that is, temperature and pH) (EFSA 2011). Even if appropriate procedures are introduced to prevent the formation of BAs, the threat of the accumulation of these compounds remains. This can occur in the presence of nonstarter LAB with BA-producing ability, which continue to grow and metabolize, for example, when the applied level of starter culture is too low or inoculated microorganisms do not overgrow indigenous ones (EFSA 2011; Świder et al. 2023). The undesired growth of Gram-negative enterobacteria at the beginning of the fermentation process represents another risk. These microorganisms are sensitive to low pH (Stoll et al. 2021) and thus, their development can occur under improper acidification. Many representatives of Enterobacteriaceae and other Gram-negative bacteria have been reported to possess the ability to produce BAs (Lorenzo et al. 2010; Meng et al. 2022; Wunderlichová et al. 2014). In contrast, the decarboxylase and deiminase reactions, in which BAs are formed, are the main physiological responses of bacteria to acidic environments (Gardini et al. 2016; Zuljan et al. 2016). Because of the complexity and variability of the fermentation process, a wide range of BA concentrations has been reported for various fermented products. Published data frequently reveal a significantly high content of BAs, exceeding estimated safety limits (Fong, El-Nezami, and Sze 2021; Shukla et al. 2010). Świder et al. (2020) reported that consumption of fermented vegetables, such as Brussel sprouts, broccoli, kimchi, cucumber, white, and red cabbage, available on the Polish retail market, pose a risk of adverse symptoms because of high BA concentrations. Commercial douchi (fermented black beans/soybeans) products contain up to 814.2 mg/kg of histamine and 643.5 mg/kg of tyramine (Fong et al. 2020), whereas the concentrations of these amines in selected samples of Doenjang (fermented soybean paste) reached 2794.8 mg/kg and 6616.1 mg/kg, respectively (Shukla et al. 2010). The reported concentrations of tryptamine, phenylethylamine, putrescine, cadaverine, agmatine, spermidine, and spermine were 2808.1, 8704.6, 4292.3, 3235.5, 5508.4, 8804.0, and 9729.5 mg/kg, respectively; however, most of the samples tested contained BAs at levels below the limit of detection (Shukla et al. 2010). This example illustrates the importance of providing efficient, repeatable methods to ensure stable, low BA levels in fermented products. Several studies have summarized the available data on BA concentrations in fermented products (Mah et al. 2019; Vasconcelos et al. 2021; Visciano and Schirone 2022).

Methods to reduce BAs in fermented products

Alterations in the microbial profile of the product, particularly the inhibition of the growth of BA-producing microorganisms and/or promotion of BA-degrading microorganisms, are the primary mechanisms of BA content reduction in fermented food systems (Jaguey-Hernández et al. 2021). Such effects can be achieved through the application of suitable starter cultures, modification of manufacturing and storage conditions (NaCl concentration and temperature), or the addition of bioactive substances. Some technological processes, such as high hydrostatic pressure, vacuum or modified atmosphere packaging, and irradiation, effectively limit BAs in fermented meat products (Jaguey-Hernández et al. 2021; Kim et al. 2005; Simon-Sarkadi et al. 2012; Sun et al. 2019); however, these methods are excluded from some fermented food matrices, because of their traditional characteristics. Household manufacturing has a similar limitation. The methods described in the literature for reducing BAs in fermented products are shown in Figure 2.

Figure 2. Methods to reduce BAs in fermented products. Created with canva.com.

Several studies have reported the successful use of starter cultures to limit BA content in fermented food products (Cheng, Xu, and Lan 2020; Kim et al. 2019; Zhao et al. 2020). Articles by Alvarez and Moreno-Arribas (2014), Jaguey-Hernández et al. (2021), and Lorenzo, Munekata, and Domínguez (2017) summarize the available data concerning this issue. It is remarkable that the value of the fermented product can be further ameliorated by the application of probiotic strains as starter cultures. Fong et al. (2020) obtained reduced tyramine content (down to undetectable values) in douchi, a black bean fermented product, because of the application of probiotic strains (Lacticaseibacillus rhamnosus GG, Lacticaseibacillus casei Shirota or E. coli Nissle 1917) whereby the features of the used strains contributed to the observed effects, as well as the environmental factors, including temperature and availability of oxygen (Fong et al. 2020). Recently, it was reported that LAB postbiotics can limit BA production by food-borne pathogens. The authors suggested that the main factors contributing to this effect were the degradation of BAs or inhibition of BA production by the tested microorganisms, namely E. coli ATCC 25922 and Salmonella Paratyphi A NCTC 13. Suppression of pathogen activity was a consequence of antimicrobial features of LAB postbiotics, and such antimicrobial effects resulted from the high content of organic acids that lowered pH. Another feasibly contributing factor pointed out by the authors was the presence of bacteriocins (Yilmaz et al. 2022). Another strategy to reduce BA concentration in fermented products was the application of modified yeast with the removed PEP4 gene encoding an enzyme, proteinase A, which is responsible for FAA production. Decreased activity of this enzyme resulted in the limited availability of BAs’ precursors, and consequently, fermented rice wines produced with modified Saccharomyces cerevisiae cells contained reduced concentrations of tyramine, histamine, and cadaverine by 57.5, 54.3, and 24.6%, respectively (Guo et al. 2015).

Some authors have indicated that the application of plant additives is an effective way to limit BA accumulation. Essential oils (EOs) can significantly enhance the microbiological quality of food and thus extend the shelf life of perishable products. They exhibit strong antimicrobial activity and counteract lipid oxidation in seafood products (Hassoun and Çoban 2017). Positive effects have been observed for rosemary (Ozogul et al. 2017) and basil EOs (Karoui and Hassoun 2017), garlic EO (Mahmoud et al. 2004), thyme and laurel EOs (Erkan et al. 2011; Ozogul et al. 2017), ginger oil (Emir Çoban 2013), clove oil (Emir Çoban and Patir 2013), orange leaf EO (Alparslan et al. 2016), and sage (Ozogul et al. 2017). The application of clove, cumin, or spearmint EOs resulted in a decrease in bacterial and yeast numbers during cold storage of red drum fillets, and consequently, a reduction in BA content, particularly histamine, putrescine, and cadaverine. Additionally, the aforementioned EOs improve the sensory characteristics of the product (Cai, Cao, et al. 2015). Interestingly, according to Zhang et al. (2018), phenolic acids applied at concentrations that do not affect bacterial growth can inhibit the formation of histamine, tyramine, putrescine, and cadaverine through Enterobacter aerogenes. Of the five compounds tested (chlorogenic, gallic, catechinic, shikimic, and protocatechuic acids), catechinic acid was the most effective in limiting BA production (Zhang et al. 2018). Such an effect could be the result of the direct inhibition of amino acid decarboxylases. Rodríguez-Caso et al. reported the inhibitory effect of green tea (-)-epigallocatechin-3-gallate (EGCG) on histidine decarboxylase. The mechanism putatively consists of modification of the holoenzyme structure (Rodríguez-Caso et al. 2003). Although this experiment was conducted on mammalian enzymes, it can be conjectured that similar effects can occur in bacterial cells.

Effect of plant-origin additives on BA concentration in fermented foods

In vitro studies

Several researchers have studied the effects of plant additives on BA accumulation in culture media (Mah, Kim, and Hwang 2009; Montanari et al. 2022; Wendakoon and Sakaguchi 1993). Food amine producers were cultured in the presence of natural compounds to assess the influence of additives on bacterial growth and BA production. Although the results of such experiments may preliminarily evaluate the prospective effects in food matrices, there is limited literature on this subject. The available information is summarized in Table 1. Some researchers have examined the growth of BA producers subjected to natural plant compounds, without quantitatively assessing BA accumulation (Kim et al. 2014; Oh et al. 2012; Zhou et al. 2016). Table 2 presents the results of these studies.

Table 1. Antimicrobial activity of plant compounds and their effects on BA accumulation - in vitro studies.

Plant material		Extraction solvent	Culture medium for BA accumulation testing	Method for the determination of antimicrobial activity	Target microorganisms	Main effects on BA content in the culture	Reference
Common name	Scientific name
Clove	Syzygium aromaticum L.	Direct addition of sterile clove powder	Mackerel (Scomber japonicus) extract supplemented with NaCl (1 or 2%)	Total plate count method	Enterobacter aerogenes ATCC 43175 (histamine-producing)	Tested concentration of clove amounted to 0.5%.After 24 h of culturing, in medium supplemented with 1% NaCl histamine concentration was almost two-fold lower because of clove addition, while in the medium containing 2% of NaCl, the production of this amine was entirely inhibited.Likewise, cadaverine production was totally suppressed in the bacteria cultured in 2% NaCl medium supplemented with clove. In the culture containing 1% NaCl, cadaverine was at the similar level regardless of clove addition.Culturing of E. aerogenes ATCC 43175 in the medium containing 2% NaCl and clove resulted in bacteria growth reduced by 8 or 7 log orders in comparison to culturing in the medium containing 2% of NaCl or 0.5% of clove alone, respectively.	Wendakoon and Sakaguchi 1993
GingerGarlicGreen onionRed pepperClovesCinnamon	Zingiber officinale Roscoe Allium sativum L. Allium fistulosum L. Capsicum annuum L. Syzygium aromaticum L. Cinnamomum cassia L.	Ethanol/water (95/5 v/v)	TSB (tryptic soy broth) supplemented with 0.5% L-histidine hydrochloride monohydrate, L-tyrosine, L-ornithine hydrochloride, L-lysine hydrochloride, and 0.0005% pyridoxal-HCl	Agar diffusion test	Four isolates of the Bacillus licheniformis species (i.e., No. 1043, 1056, 1542 – strong producers of histamine, putrescine and cadaverine, and No. 1553 – strong producer of histamine, tyramine, and putrescine) originated from Myeolchi-jeot (fermented anchovy)	Application of 1 mL of garlic extract (ca. 16%) resulted in the reduction of putrescine, cadaverine, histamine, and tyramine concentrations by 11.2%, 18.4%, 11.7%, and 30.9%, respectively, compared to control culture. Application of 0.5 mL of this extract (ca. 8%) inhibited spermidine formation the most efficiently − 17.4% reduction. For remained tested extracts obtained reduction of BAs in experimental culture medium was as follows:- green onion: 33.28% for tyramine (0.5 mL addition) and 10.87% for spermidine (1.0 mL)- red pepper: 10.73% for cadaverine, 32.49% for tyramine, and 27.34% for spermidine (0.5 mL)- ginger: 12.77% for putrescine (1.0 mL), 26.27% for tyramine (0.5 mL), and 27.17% for spermidine (0.1 mL)- cinnamon: 20.57% for putrescine (0.1 mL) and 23.66% for tyramine (0.5 mL)- cloves: 28.30% for tyramine (0.1 mL) and 19.82% for spermidine (1.0 mL). Moreover, the extract of garlic showed the highest antimicrobial activity against the amine producers tested.	Mah, Kim, and Hwang 2009
BlackberryJuniper	Rubus fruticosus L. Juniperus oxycedrus L.	Extraction of phenolics (PEs) and essential oils (EOs)PEs: 50% ethanol using the MAE (advanced microwave extraction system)EOs: hydrodistillation; pentane and diethyl ether (1:1 v/v) were used for trapping the volatile compounds	BHI (brain heart infusion broth)	MIC by broth microdilution method	Enterococcus faecium strain FC12 (tyramine-producing) originated from cheese	Plant additives were applied at sub-lethal concentrations (50% of MIC), namely 1 mg/mL except for R. fruticosus L. EO, that was added at concentration 0.75 mg/mL. Accumulation of tyramine followed the growth kinetics of tested bacteria. After 96 h of the culturing, tyramine content was in the range from ca. 120 mg/L (cultures with the EOs) to ca. 160 mg/L (control culture), so its maximum reduction reached approx. 25%. 2-phenylethylamine concentration ranged from ca. 15 mg/L (culture with R. fruticosus L. EO) to 85.3 mg/L (control), which represents approx. 82% reduction.The EOs showed a higher antimicrobial effect than PEs (especially R. fruticosus L. added at 0.75 mg/mL), what was confirmed in flow cytometry.	Montanari et al. 2022

Table 2. Antimicrobial activity of plant compounds against BA-producing bacteria - in vitro studies.

Plant material		Extraction solvent	Method for the determination of antimicrobial activity	Target microorganisms	Main antimicrobial effects in the culture	Reference
Common name	Scientific name
GarlicGingerCinnamon Star anise	Allium sativum L. Zingiber officinale Roscoe Cinnamomum cassia L. Illicium verum L.	Ethanol/water (95/5 v/v)	Agar diffusion test	Enterobacter cloacae isolate 17, Citrobacter freundii isolate 27, and Klebsiella pneumoniae isolate 54 – BA producers isolated from fish sauce	No tested additive exhibited antibacterial activity against E. cloacae.Garlic and star anise extracts significantly inhibited K. pneumoniae and C. freundii, respectively.	Zhou et al. 2016
Six species of brown algae	Ecklonia cava Eisenia bicyclis Sargassum sagamianumSargassum thunbergiiMyagropsis myagroidesSargassum horneri	Dried and milled algae were extracted with 94% ethanol or water at a ratio of 1:10 (w/v)	Disk diffusion method and minimum inhibitory concentration (MIC) test	Morganella morganii IFO 3848, ATCC 25830 – histamine producer	An Ecklonia cava ethanol extract (ECEE) exhibited the strongest antimicrobial activity (MIC = 2 mg/mL), as well as inhibitory effect against the activity of crude histidine decarboxylase of M. morganii (reduction by 33.79%; ECEE concentration: 1 mg/mL).The ethanolic extract of Eisenia bicyclis and Sargassum thunbergii also significantly reduced the activity of the tested enzyme (19.82 and 12.91%, respectively).	Kim et al. 2014
Schizandra chinensis Baillon (SCB) Prunus mume Siebold et Zuccarini (ZUCCA) Rosmarinus officinalis L. (RO) Thuja orientalis Rosa Polyphenol of green tea (PGT)Grapefruit seed extract (GSE) Glycyrrhiza uralensis (GU) Prunus mume Siebold & Zucc. (ZUCC)		Ethanol/water (70/30 v/v) extraction, vacuum-evaporation and freeze drying.PGT and GSE were commercial samples	Agar diffusion test (ADT) and minimum inhibitory concentration (MIC) tests	Enterococcus faecium – tyramine producer isolated from Cheonggukjang – a traditional Korean fermented soy food	SCB, ZUCCA, GU, ZUCC, GSE, and PGT exhibited strong antimicrobial activity against E. faecium, based on the ADT. According to the MIC test, the extracts of SCB, ZUCC, RO, PGT, and GSE were more potent antimicrobial substances (≤ 5 mg/mL) than ZUCCA, GU, Thuja orientalis, and Rosa(≤ 10 mg/mL).	Oh et al. 2012

Application to food matrices

Data on the application of plant-derived additives to fermented products are summarized in Tables 3–6. The experimental results varied depending on the matrix, additive, and application conditions. The production stage at which the additives were applied (Lee et al. 2018; Shukla et al. 2019), as well as the size (that is, sausage diameters) of the products (Huang et al. 2021) also significantly contributed to the obtained results. Most studies (27 of 38) were related to the reduction of BAs in fermented products of animal origin, such as meat (19), fish and seafood (5), and dairy products (3). Twelve articles reported plant-based fermented foods, including soybeans, cereals, sauerkraut, kimchi, and bread. Tables 3–6 show the effects of plant-origin additives on the BA content in meat, fish and seafood, dairy, and plant-based fermented products, respectively.

Table 3. Effect of plant-origin additives on BAs in fermented meat products.

Fermented product	Applied plant additive and its dose	Form of additive	Main effects on BA content	Reference
Fermented mutton sausage	Spices extracts:star anise amomum tsao-ko clovecassiafennelbay leaf nutmeg	ethanolic extracts (95% ethanol) evaporated and dissolved in water	The greatest reduction of tyramine and histamine was obtained in the samples with clove extract addition − 18.7 and 9.6% in comparison to control, respectively. Clove extract was the most efficient also regarding 2-phenylethylamine and tryptamine – reduction by 21.8 and 24.6%, respectively. Spermidine and putrescine were reduced by 27.5 and 19.3%, respectively, because of cassia addition.	Jia et al. 2020
Dry fermented pork sausages	Salvia hispanica (Chia) seed (1 or 2%) Nigella sativa (Black Cumin) seed (1 or 2%)	grounded seeds, particle size <0.3 mm	Significantly increased tyramine and putrescine concentrations in comparison to control, as well as reduced spermine concentration.Application of 2% of chia seed significantly increased spermidine content.Agmatine content was reduced to values below limit of detection.	Borrajo et al. 2021
Smoked horse meat sausage	Thyme essential oil	purchased	Application of thyme essential oil significantly reduced putrescine (by 13% bigger diameter and by 22% smaller diameter), cadaverine (23% and 24%, respectively), histamine (24% and 33%, respectively) and tyramine content (17% and 18%, respectively), as well as total BAs (16% and 18%, respectively).Spermidine content increased by 16% (bigger diam) and 10% (smaller diam), while spermine increased by 3% either in the sausages of bigger or smaller diameter.	Huang et al. 2021
Smoked horsemeat sausage	Thyme essential oil (at concentration 0.156%) + Proteus bacillus starter cultureThyme microcapsules (at concentration 0.156%) + Proteus bacillus starter culture	purchased	Application of thyme microcapsules or thyme essential oil resulted in the significant reduction of histamine content by 66.15 or 49.22%, respectively, in comparison to control.Use of thyme microcapsules was more efficient and reduced histamine concentration by 33.35% compared to the samples with thyme essential oil.	Yu et al. 2021
Fermented pork sausages	Rose polyphenols at concentrations:1 mg/g meat2 mg/g meat3 mg/g meat	vacuum dried water extracts	Application of 3 mg/kg of rose polyphenols (RPs) resulted in a significant reduction of phenylethylamine, putrescine, and histamine in comparison to control (without rose polyphenols) and other variants after 24 d of fermentation.Addition of RPs at the levels of 2 mg/g or 3 mg/g significantly decreased tyramine concentration.Addition of RPs at the levels of 1, 2 or 3 mg/g significantly reduced cadaverine and spermidine contents.	Zhang et al. 2017
Sucuk – Turkish dry-fermented sausage	Urtica dioica extract:300 mg/kg600 mg/kg Hibiscus sabdariffa extract:300 mg/kg600 mg/kg	aqueous extracts	Application of 300 mg/kg of Urtica dioica extract reduced histamine, putrescine, and tyramine concentrations by 62.86, 91.12, and 14.42%, respectively, in comparison to control, after 15 days of fermentation.Application of 600 mg/kg of Urtica dioica extract reduced histamine, putrescine, and tyramine contents by 70.19, 90.41, and 19.49%, respectively.Addition of 300 mg/kg of Hibiscus sabdariffa extract reduced histamine, putrescine, and tyramine concentrations by 46.43, 82.59, and 27.35%, respectively.Addition of 600 mg/kg of Hibiscus sabdariffa extract reduced histamine, putrescine, and tyramine by 40.85, 76.91, and 21.50%, respectively.	Karabacak and Bozkurt 2008
Turkish dry-fermented sausage	Thymbra spicata oil 300 ppmSesame (Sesamum indicum L.) oil 300 ppm	essential oil obtained by steam distillation of air dried Thymbra spicata, dried over anhydrous sodium sulfate purchased roasted sesame oil	Application of Thymbra spicata oil and sesame oil decreased putrescine content by average 34.89 and 27.7%, respectively, in comparison to control, after 16 days of fermentation. Histamine concentration was reduced by 12.60 and 8.65%, respectively, while tyramine by 12.87 and 13.50%, respectively. Applied additives reduced analyzed BAs more efficiently than BHT – an antioxidant commonly used in the food industry.	Bozkurt 2007
Sucuk – Turkish dry-fermented sausage	Green tea extract 300 ppm Thymbra spicata oil 300 ppmGreen tea extract 150 ppm + Thymbra spicata oil 150 ppm	water green tea extract essential oil obtained by steam distillation of air dried Thymbra spicata, dried over anhydrous sodium sulfate	Application of green tea extract, Thymbra spicata oil or mix of them reduced average putrescine content during 15 d of fermentation by 34.42, 22.70, and 29.21%, respectively, in comparison to control.After 15 d of fermentation histamine concentration was the lowest in the samples with green tea extract. Application of Thymbra spicata oil or mixed T. spicata and GTE also resulted in the decrease of histamine content to ca. 200 ppm, while the concentration of this amine in the control sample was 275.3 mg/kg.Tyramine content was reduced by 24.25% because of the application of green tea extract.Examined additives reduced analyzed BAs contents more efficiently than BHT.	Bozkurt 2006
Harbin dry sausage	Seasonings extracts at concentration 0.3 g/kg:cinnamoncloveanise	ethanolic extracts (95% ethanol) concentrated with removal of ethanol, then freeze-dried and ground into a powder	Application of the extracts significantly reduced the content of six analyzed BAs in comparison to control, whereby the biggest difference compared to the other variants was obtained thanks to cinnamon extract use.The efficiency in BAs reduction of tested extracts was as follows: cinnamon > anise > clove. In comparison to control, after 9 d of fermentation, addition of cinnamon extract resulted in the reduction of putrescine by 18.93%, while cinnamon, anise, and clove extracts reduced histamine content by 21.89, 17.42, and 13.44%, respectively.	Sun et al. 2018
Fermented pork sausage	Tea polyphenol 0.3%Ginger essential oil 0.3%Anise essential oil 0.3%Cinnamon essential oil 0.3%	purchased	Anise EO was the most effective in the limitation of histamine, putrescine, tyramine and cadaverine formation.Reduction of histamine content by 31.9, 34.74, 28.22, and 19.02% because of application of ginger, anise, cinnamon EOs, and tea polyphenols, respectively.Reduction of tyramine content by 16.64, 23.76, 15.55, and 10.12% because of application of ginger, anise, cinnamon EOs, and tea polyphenols, respectively.Reduction of putrescine content by 39.31% due to addition of anise EO.Reduction of cadaverine content by 40.53, 42.68, 20.68, and 29.83% because of application of ginger, anise, cinnamon EOs, and tea polyphenols, respectively.Significant reduction of total content of 4 analyzed BAs by 28.58, 34.87, 18.58, and 21.31% in comparison to control because of application of ginger, anise, cinnamon EOs, and tea polyphenols, respectively.	Wang et al. 2021
Traditional Chinese smoked horsemeat sausage	plant extracts: tea polyphenols 0.19% and essential oils of cinnamon 0.025%, cloves 0.04%, ginger 0.024%, and anise 0.025%starter cultures (Lactobacillus sakei and Staphylococcus xylosus) + plant extracts (tea polyphenols 0.19% and essential oils of cinnamon 0.025%, cloves 0.04%, ginger 0.024%, and anise 0.025%)	EOs produced by supercritical CO2 extraction tea polyphenols – purchased	BA levels were reduced stronger by plant extracts than starter cultures applied alone. Synergistic effects were noticed when plant extracts and starter cultures were applied together.After 28 d of ripening:Tryptamine concentration was reduced by 23.76 and 74.92%; 2-phenylethylamine by 30.15 and 33.70%; putrescine by 71.97 and 84.97%; cadaverine by 75.37 and 81,00%; histamine by 36.48 and 100%; tyramine by 84.84 and 90.70%, when plant extracts and combination of plant extracts + starter cultures were applied, respectively. No significant differences occurred concerning spermine content. In comparison to control, spermidine concentration was higher by 10.31% in the samples with plant extracts addition and higher by 9.16% when plant extracts + starter cultures were applied.After 4 months of storage vacuum or non-vacuum packaged:Higher reduction of the content of tryptamine, 2-phenylethylamine, putrescine, and cadaverine after storage in vacuum package. Percentage reduction of aforementioned BAs was as follows: 56.96, 76.03, 86.04, and 70.51% in the variant with plant extracts alone, and 71.51, 77.07, 91.27, and 70.47% when both plant extracts and starter cultures were applied.Histamine reduction was the highest (93.52% in comparison to control) when both plant extracts and starter cultures were added, and the product was stored in vacuum package. In the variant where plant extracts were applied alone the reduction of histamine was higher in non-vacuum-packed product (50.99% compared to control).Tyramine reduction was the highest (90.28% in comparison to control) when both plant extracts and starter cultures were added, and the product was stored in non-vacuum package. In the variant where plant extracts were applied alone the reduction of tyramine was higher in vacuum-packed product (77.50% compared to control).Spermine contents were higher than in control, when plant extracts alone were applied both in vacuum and non-vacuum packaged sausages, 10.37 and 12.98% respectively. The highest reduction of spermine resulted from application of plant extracts in combination with starter cultures and vacuum-packaging (55.54% in comparison to control).Spermidine content was reduced the most (9.85% in comparison to control) when plant extracts were applied alone, and the product was stored in non-vacuum package.	Lu et al. 2015
Fermented sausage	Cava lees 5%Cava lees 5% + L. sakei CTC494Cava lees phenolic extract 0.3%Cava lees phenolic extract 0.3% + L. sakei CTC494Cava lees phenolic extract 0.3% + L. sakei BAP110	liquid DMSO phenolic extract prepared through water: ethanol (50:50) extraction of lyophilized, ground cava lees	After 21 days of ripening:Due to the addition of 5% Cava lees to spontaneously fermented sausages tyramine and cadaverine contents were reduced by 100% and 76.50%, respectively. Putrescine, spermidine and spermine contents were not altered significantly, while histamine was not detected.Samples contaminated with aminogenic Salmonella strains producing cadaverine, putrescine and histamine; after 21 days of ripening:In spontaneous fermentation, 5% addition of Cava lees resulted in the reduction of cadaverine and putrescine by 62 and 78%, respectively. Tyramine content was not altered significantly.Inoculation with non-aminogenic L. sakei CTC494 strain resulted in absence, or low BAs content, regardless of the addition of Cava lees.In spontaneous fermentation, the addition of 0.3% cava lees phenolic extract resulted in the reduction of cadaverine and putrescine concentrations by 21 and 40%, respectively. Tyramine content was not altered significantly.Inoculation with non-aminogenic L. sakei CTC494 strain inhibited the production of putrescine, cadaverine, and tyramine regardless of cava lees extract addition.Inoculation with non-aminogenic L. sakei BAP110 inhibited the formation of cadaverine and putrescine regardless of cava lees extract addition. Tyramine was not reduced completely either in the control (inoculated with L. sakei BAP110) or enriched with cava lees extract sample (L. sakei BAP110 + 0.3% cava lees extract). Its content was at similar level in both variants.	Hernández-Macias et al. 2021
Nham: fermented pork product	Ginger extract (20%) 34.4 U/g amine oxidase activity	minced ginger	Total biogenic amines content was reduced by 85.90% compared to control, after 7 d of fermentation. Putrescine, cadaverine, histamine, and tyramine were reduced by 95.31, 92.62, 79.32, and 79.76%, respectively.	Kongkiattikajorn 2015
Smoke – cured bacon	Grape seed extract 1 g/kg	purchased	In comparison to control, addition of grape seed extract resulted in the reduction of tyramine, cadaverine, putrescine, 2-phenylethylamine, and histamine concentration by 30.7, 37.1, 29.4, 34.5, and 73.6%, respectively.	Wang, Zhang, and Ren 2018
Aeros thasou – traditional fermented pork sausage (Greece)	Satureja thymbra EO (5 g/kg) + L. sakei	no data	In comparison to control, concentrations of tyramine, putrescine, and histamine were reduced by 62, 100, and 71%, respectively.	Latorre-Moratalla et al. 2010
Beef sausages	Punica granatum L. 1% Salvia eremophila 1%	Extraction of the ground peel of P. granatum or aerial parts of S. eremophila with aqueous methanol (80% v/v) in the absence and presence of acetic acid (HOAc, 5% v/v), filtration and vacuum-concentration	After 14 days of ripening samples supplemented with P. granatum extract contained the highest concentration of histamine, cadaverine, and putrescine among the tested variants. The levels of those BAs were ca. 2.6 times higher than in the samples without extracts, supplemented with 120 ppm of nitrite, that contained the lowest level of examined BAs.Samples fortified with S. eremophila extract contained ca. 1.5 times higher concentrations of tested BAs.Application of each extract individually in combination with 60 ppm of nitrite was more effective regarding inhibition of BAs accumulation compared to the application of plant extracts alone.	Abedi et al. 2023
Chinese sausages	Tea polyphenol (TP) 0.05% (g/g)Epigallocatechin gallate (EGCG) 0.05% (g/g)palmitoyl-TP (pTP) 0.05% (g/g) palmitoyl-EGCG (pEGCG) 0.05% (g/g)	purchased, powder	In comparison to control, after 2 days of fermentation and 4 wk of ripening:The total concentration of six analyzed BAs was reduced by 22.64, 36.89, 44.15, and 55.08% in the samples supplemented with TP, EGCG, pTP, and pEGCG, respectively.Application of pEGCG was the most effective regarding putrescine, tyramine, spermine, and spermidine. Their contents were reduced by 40.52, 61.25, 44.17, and 40.02%, respectively. Additionally, the concentrations of cadaverine and histamine in the samples with pEGCG decreased by 74.02 and 3.89%, respectively.Histamine content was reduced the most efficiently in the samples fortified with TP (9.22%), while cadaverine in pTP group (ca. 10 times lower than in control).	Zhou, Mo, Tang, et al. 2023
Chinese sausages	Tea polyphenol (TP) 0.05% (g/g) Epigallocatechin gallate (EGCG) 0.05% (g/g) palmitoyl-TP (pTP) 0.05% (g/g) palmitoyl-EGCG (pEGCG) 0.05% (g/g)	purchased	In comparison to control, after 23 days of fermentation:Total BAs content was reduced by 47.41, 37.17, 37.19, and 26.24% in the samples fortified with EGCG, pEGCG, pTP, and TP, respectively.EGCG and pEGCG were the most efficient regarding tyramine (reduced by approx. 41%), as well as histamine and putrescine contents reduction, while pTP addition resulted in the lowest content of spermidine.Cadaverine concentration was reduced by 76.72, 80.23, 88.53, and 63.51% following fermentation with TP, EGCG, pTP, and pEGCG, respectively.Spermine content was reduced by 20.66, 46.64, 28.51, and 27.13% in TP, EGCG, pTP, and pEGCG groups, respectively.2-phenylethylamine content decreased to not detected values in each treatment group.	Zhou, Mo, Wang, et al. 2023
Smoked horsemeat sausage	Coreopsis tinctoria Nutt. essential oil (CEO): 0.312% Coreopsis tinctoria Nutt. essential oil microcapsules (CEOM): 0.312%	purchased	In comparison to control, after 28 days of fermentation:Histamine was reduced by 63.37% and 80.42% in the samples supplemented with CEO and CEOM, respectively.Tyramine was reduced by 58.22% and 65.25% in the samples supplemented with CEO and CEOM, respectively.Putrescine was reduced by ca. 35.00% and 62.04% in the samples supplemented with CEO and CEOM, respectively.Cadaverine content was ca. 3 and 6 times lower in CEO and CEOM groups, respectively.Tryptamine content was ca. 1.5 and 2 times lower in CEO and CEOM groups, respectively.There was no significant difference regarding concentrations of spermine, spermidine and 2-phenylethylamine.	Li et al. 2023

Table 4. Effect of plant-origin additives on BAs in fermented fish and seafood.

Fermented product	Applied plant additive and its dose	Form of additive	Main effects on BA content	Reference
Myeolchi-jeot fermented anchovy	Garlic extract	ethanolic extract (95% ethanol)	In a model system the total content of analyzed BAs in the samples with garlic extract was reduced by 8.7% compared to control.	Mah, Kim, and Hwang 2009
Fermented fish sauce	Ethanolic extracts of:GingerGarlicCinnamonStar anise	ethanolic extracts (95% ethanol)	In comparison to control, garlic and star anise extracts significantly reduced histamine content by 30.49 and 8.09%, respectively, while application of ginger or cinnamon extracts increased histamine concentration by 4.82 and 13.36%, respectively.Ginger, garlic, and star anise extracts significantly reduced putrescine concentration by 11.79, 17.65, and 32.24%, respectively. Application of cinnamon extract resulted in the decrease of putrescine content by 3.22%.Tyramine concentration was reduced significantly by 26.03 and 22.79%, because of star anise and garlic extracts application, respectively. The use of cinnamon or ginger extracts reduced tyramine concentration by 2.92 or 13.12%, respectively.Addition of garlic, ginger, and star anise extracts reduced spermidine content by 37.20, 33.45, and 27.25%, respectively. Application of cinnamon extract reduced spermidine content by 5.65%.Total amount of four BAs was significantly reduced by 27.17, 23.25, and 13.49% thanks to application of garlic, star anise, and ginger ethanolic extracts, respectively.	Zhou et al. 2016
Fermented sardine	Plant + cell-free extracts from LAB:thyme extract + cell-free extract from Lactobacillus plantarum FI8595 (TH-LP)thyme extract + cell-free extract from Pediococcus acidolactici ATCC 25741 (TH-PA) laurel extract + cell-free extract from Lactobacillus plantarum FI8595 (LA-LP)laurel extract + cell-free extract from Pediococcus acidolactici ATCC 25741 (LA-PA)	plant extracts obtained through carbon dioxide supercritical fluid extraction water cell-free extracts	The use of thyme extract with cell-free extract from Pediococcus acidolactici ATCC 25741 resulted in lower cadaverine concentration compared to the control and other variants after 8 wk of storage.After 8 wk, putrescine reached the highest value in TH-LP combination, while the lowest content of this BA was obtained in LA-PA variant.After 8 wk, spermine concentration was the lowest in LA-LP and LA-PA and the highest in TH-LP. Spermidine was present in smaller amounts, the highest value after 8 wk of storage was measured in TH-LP variant.Histamine content was insignificantly higher in PA after 8 wk of storage.Similarly, tyramine concentration was the highest in PA after 8 wk, while significantly lower in LP.Plant extracts induced lower concentrations of dopamine and serotonin after 8 wk of storage.	Kuley et al. 2018
Shrimp paste	tea polyphenols 0.3% 6-gingerol 0.3% tea polyphenols 0.15% + 6-gingerol 0.15%	purchased	The combination of tea polyphenols (0.15%) and 6-gingerol (0.15%) was the most effective in inhibiting the formation of BAs. After 160 d of storage the contents of putrescine, cadaverine, histamine, phenylethylamine, tryptamine, and tyramine were reduced by 75.05, 62.82, 72.89, 68.17, 61.00, and 65.85%, respectively, compared to control.Application of tea polyphenols or 6-gingerol alone also resulted in a significant reduction of BAs in comparison to control. 6-gingerol was even more effective than tea polyphenols regarding the concentrations of cadaverine, histamine, and tyramine. It reduced the content of aforementioned BAs by 59.15, 68.17, and 62.97%, respectively. The concentrations of putrescine, phenylethylamine, and tryptamine were reduced by the addition of 6-gingerol by 67.70, 59.03, and 54.01%, and did not differ significantly from the values obtained when tea polyphenols alone were applied.The application of tea polyphenols alone resulted in the reduction of putrescine, cadaverine, histamine, phenylethylamine, tryptamine, and tyramine by 63.64, 55.48, 63.06, 58.75, 56.06, and 59.79%, respectively.Spermine and spermidine were not detected in shrimp paste samples during the experiment.	Cai, Liu, et al. 2015
Chouguiyu – fermented fish product	Papain:10 U/g50 U/g200 U/g400 U/g	purchased	Addition of papain significantly reduced BA concentration in comparison to control (no papain addition) regardless of applied dose. Application of 200 U of papain per 1 g of fish reduced total BA content by 89.47% and was the most efficient amongst tested variants.	Xu et al. 2022

Table 5. Effect of plant-origin additives on BAs in fermented dairy products.

Fermented product	Applied plant additive and its dose	Form of additive	Main effects on BA content	Reference
Gouda cheese	Zataria multiflora Boiss. essential oil:0.05% v/v0.1% v/v0.2% v/v0.4% v/v	EO of air-dried aerial parts of Z. multiflora	After 90 days of ripening significant reduction of tyramine and histamine in comparison to control occurred in the samples where 0.1, 0.2 or 0.4% of EO were applied. The higher the concentration of EO added, the greatest the reduction of analyzed BAs. Tyramine content was reduced by 5.05, 21.94, and 34.40%, while histamine content was reduced by 14.00, 29.61, and 46.60% in the samples with 0.1, 0.2, and 0.4% of EO addition, respectively.	Es’haghi Gorji et al. 2014
Unripened curd cheese	Fermented plants at the concentration of 3% w/v: Satureja montana L. sakei:Traditional submerged fermentation (SMF)Solid state fermentation (SSF) P. acidilactici SMFSSF P. pentosaceus SMFSSF Rhaponticum carthamoides L. sakei SMFSSF P. acidilactici SMFSSF P. pentosaceus SMFSSFNon-fermented plants: Satureja montana Rhaponticum carthamoides	fermented plants: liquid fermented LAB bioproducts prepared with the use of dried, ground plants Non-fermented plants: dried and ground to particle size of 0.5 − 2.0 mm	Either type of plant, bacteria strain or type of fermentation affected the content of BAs in the final product.Generally, both fermented and non-fermented plants addition resulted in a higher total BA concentration in cheese than in control samples – without plant additives.Cadaverine contributed most to the total BAs content in all samples with fermented plants addition, as well as in the sample with non-fermented Rhaponticum carthamoides.The highest total BA content was analyzed in cheese with the addition of Rhaponticum carthamoides fermented with L. sakei under traditional submerged fermentation conditions and was above 500 times higher than in control. Cadaverine represented above 80% of the sum of 8 analyzed BAs in the aforementioned sample.The lowest concentration of total BAs amongst the samples with plant additives was obtained in cheese with Rhaponticum carthamoides fermented with L. sakei under solid state fermentation and was almost 11 times higher than in control.Tyramine was absent in almost all samples with plant additives.The highest histamine concentration was analyzed in the sample with non-fermented Satureja montana addition and reached 25.17 mg/kg.	Mozuriene et al. 2016
Cheddar cheese	Bunium persicum Boiss. essential oil (BPEO) [% (v/v)]:0.050.10.20.4	hydrodistillation of EO	The higher the BPEO concentration, the more effectively BA accumulation was inhibited.In comparison to control, after 90 days of ripening histamine and tyramine contents were reduced by 48.59% and 35.94%, respectively, in the samples containing 0.4% BPEO.	Raoofi, Noori, and Khanjari 2023

Table 6. Effect of plant-origin additives on BAs in plant-based fermented food.

Fermented product	Applied plant additive and its dose	Form of additive	Main effects on BA content	Reference
Sauerkraut	onion (350 g/kg)caraway (10 g/kg)	fresh, shredded onion caraway seeds	After 14 days of fermentation: Fermentation at 18 °C resulted in the reduction of cadaverine (by 21.77% in the samples with caraway and 54.43% in the samples with onion) and tyramine (by 45.42 and 38.79%, respectively) in comparison to control, as well as reduction of phenylethylamine (by 22.70%) in the samples with onion.Fermentation at 31 °C resulted in the reduction of tryptamine (by 59.61 and 52.51% in the samples with caraway and onion, respectively).After 12 wk of storage: significantly reduced content of cadaverine and phenylethylamine in the samples fermented at 18 °C with onion and significantly higher concentration of putrescine, cadaverine and spermidine in the samples fermented at 18 °C with caraway. Storage of samples fermented at 31 °C resulted in a significant reduction of putrescine (when caraway was added) and spermine (in the samples with onion).	Majcherczyk and Surówka 2019
Tarhana – fermented cereal product	Grapeseed extract [g/kg]:4816	powder	Application of 8 or 16 g/kg of the extract resulted in a significant reduction of putrescine (by 84% and 90%, respectively), cadaverine (to values below limit of detection), as well as total amount of analyzed BAs (by 77% and 83%, respectively) in comparison to control (without grape seed extract) after 6 months.	Akan and Ocak 2019
Fermented soybean paste	Grapefruit seed extract (300 mg/kg)Catechins (3 g/kg) –epicatechinepicatechin gallateepigallocatechinepigallocatechin gallate	purchased grapefruit seed extract catechins – powder	Addition of grapefruit seed extract resulted in a 5% reduction of total BAs and 16% reduction of putrescine content after 40 days of storage.Application of epicatechin, epicatechin gallate, epigallocatechin, and epigallocatechin gallate resulted in a reduction of total BA content by 29, 35, 44, and 37%, respectively. Putrescine concentration was reduced by 64, 60, 76, and 73%, respectively, and cadaverine by 24, 34, 42, and 37%, respectively.	Lee et al. 2018
Gangjang – Korean soy sauce	200 g of coriander per 2 kg Meju blocks	fresh coriander	Significant reduction of histamine, putrescine, and tyramine by 48.03, 43.96, and 57.74%, respectively.	Mannaa, Seo, and Park 2020
Meju – fermented soybean-based product	Allium sativum (Garlic clove):1% (GAM1)10% (GAM10) Ginkgo biloba (leaves):1% (GIM1)10% (GIM10) Nelumbo nucifera (Lotus leaves):1% (LOM1)10% (LOM10)Mix of A. sativum, G. biloba and N. nucifera (1:1:1)1% (MIM1)10% (MIM10)	ethanolic extracts	Mostly, BA concentration was higher in the samples with plant extracts addition than in control. An exception was putrescine concentration in GAM1, GAM10, and LOM1, histamine in GAM1, and GAM10, as well as spermine in GIM1, GIM10, MIM1, and MIM10. Sum of nine analyzed BAs was the highest in the LOM10 sample and was almost 6 times higher than total BAs in control. The lowest difference compared to control regarding total BAs represented GAM1 sample (0.5% higher sum of BAs).	Shukla et al. 2018
Doenjang – traditional Korean fermented soybean paste	Ground garlic:2%6%10%Heat-dried garlic:1%2%3%Freeze-dried garlic:1%2%3%	paste of fresh garlic dried garlic	After 2 months of fermentation:Reduction of the sum of 9 analyzed BAs in almost all tested variants, except 3% heat-dried garlic. Despite the highest cadaverine concentration, above 5 times higher than in control, application of 1% heat-dried garlic was the most effective in the reduction of the total BA content (by 51.34% in comparison to control). Concentration of spermidine was at similar level in all tested variants and remained in the range 1.87–1.92 mg/100g.Spermine content was reduced to not detectable value after application of 1 or 2% heat-dried garlic and 1% freeze-dried garlic.Application of 1% heat-dried garlic resulted in the greatest reduction of histamine and tyramine, by 66.24 and 86.55%, respectively, compared to control.The greatest reduction of tryptamine and putrescine, by 51.53 and 55.56%, respectively, was obtained because of an application of 3% freeze-dried garlic.Samples with 1 or 3% freeze-dried garlic were characterized by maximum reduction of cadaverine 13.19%.Application of 6% ground garlic resulted in the greatest reduction of 2-phenylethylamine content, by 37.13%.Agmatine remained below limit of detection in all tested variants.	Bahuguna et al. 2019
Kimchi	White radish ground:0 g4.5 g18 gRed pepper powder:0 g2 g8 gGarlic ground:0 g1.5 g6 gGinger ground:0 g0.25 g1 gWelsh onion ground:0 g1.5 g6 gSticky rice porridge:0 g1.75 g7 g	ground fresh white radish, garlic, ginger, and Welsh onion red pepper – powder all additives purchased from kimchi manufacturer	After 7 d of fermentation:Amongst plant additives the only one that reduced total BA content (by 4.46% in comparison to control) was red pepper powder applied at the highest level (8 g).Histamine was present in kimchi mainly due to the addition of fish sauce. None of the plant additives reduced the concentration of this BA.Tyramine concentration was reduced in the samples with zero or low white radish, zero or high garlic, low or high red pepper powder, low Welsh onion, and high sticky rice porridge addition. Amongst them the greatest reduction resulted from lack of white radish addition – decrease by 43.03% in comparison to control.Cadaverine was reduced in the samples without white radish or with high level of garlic, whereby high garlic addition was more effective. Concentration of cadaverine decreased by 28.16% in comparison to control.Content of putrescine was reduced along with zero ginger, low sticky rice porridge or high red pepper powder addition. The biggest reduction (by 42.38%) resulted from lack of ginger.Low white radish addition caused the reduction of phenylethylamine and spermidine contents by 15.38 and 9.89%, respectively, and was the most effective amongst tested combinations regarding these amines.High white radish addition reduced the content of agmatine and spermine by 30.43 and 22.71%, respectively.Tryptamine content was reduced the most when high level of sticky rice porridge was added − 34.98% less of this amine than in control.	Kim, Dang, and Ha 2022
Doenjang – fermented Korean soybean paste	Extracts-based Meju (EMD) / traditional Meju with plant extracts added later (TMD): Allium sativum (Garlic clove):1%10% Ginkgo biloba (leaves):1%10% Nelumbo nucifera (Lotus leaves):1%10%Mix of A. sativum, G. biloba and N. nucifera (1:1:1)1%10%	dried extracts obtained by freeze-dried ethanolic extraction	After 12 months of fermentation:In TMD, each plant extract caused the reduction of total BA content compared to control – without extracts.In EMD only Doenjang with 1% of garlic or lotus extracts showed higher sum of nine analyzed BAs than in control. Application of 10% garlic extract resulted in the lowest content of total BAs.	Shukla et al. 2019
Bread	Cava lees:1%2%5%	lyophilized, ground	Addition of cava lees did not alter the contents of putrescine and spermidine, regardless of applied level. Tyramine, histamine, and spermine were absent in all samples. Cadaverine was absent in control bread sample while its content reached almost 3 mg/kg in all tested variants containing cava lees.	Hernández-Macias et al. 2021
Tarhana: a cereal based fermented food	Pomegranate seed extract (PSE):0.5%1.0%2.0%	powder, purchased	Addition of 0.5, 1.0, and 2.0 % of PSE resulted in the following percentage reduction of the total BA content: 36.33, 42.49, and 52.54%, respectively.After 6 months of storage putrescine concentration was reduced significantly only when 2.0% of PSE was applied and the reduction reached 30.92% in comparison to control sample – without PSE. Cadaverine content was reduced by 13.04, 23.33, and 33.69%, while tyramine by 21.08, 24.71, and 17.85%, respectively, when 0.5, 1.0, and 2.0% of PSE was added. Significant reduction of histamine was obtained only in the samples with 0.5 or 1.0% of PSE − 19.86, and 23.0% less than in the control, respectively. Spermidine content was reduced to not detectable value in the samples supplemented with 0.5 or 2.0% of PSE. 66.68% reduction of this amine was calculated for the sample with 1.0% of PSE. There was no significant difference between samples regarding spermine concentration.	Erol and Özdestan Ocak 2020
Cheonggukjang – a traditional Korean fermented soy food	Schizandra chinensis Baillon extract (5 mg/kg) Rosmarinus officinalis L. extract (5 mg/kg) Prunus mume Siebold & Zucc (5 mg/kg) Prunus mume Siebold et Zuccarini (5 mg/kg)	extraction with 70% ethanol, vacuum-evaporation and freeze drying	In comparison to control, tyramine content was reduced by 94.74, 90.85, 86.33, and 81.93% in the samples supplemented with extracts of Rosmarinus officinalis L., Schizandra chinensis Baillon, Prunus mume Siebold et Zuccarini, and Prunus mume Siebold & Zucc, respectively.	Oh et al. 2012
Soy sauce	Phytochemicals at concentration 200 mg/kg:QuercetinRutinGallic acidFerulic acidTea polyphenol Camellia oleifera Bamboo leaf extract	Except for Camellia oleifera extract all the phytochemicals were purchased. Camellia oleifera extract was prepared through extraction with 70% (v/v) aqueous ethanol and vacuum drying via N2	After 60 days of fermentation total BA content was reduced by 24.46, 29.35, and 23.95% in the samples supplemented with quercetin, tea polyphenols, and Camellia oleifera extract, respectively. Application of other phytochemicals resulted in the lower than 20% reduction of total BAs, except for samples with rutin, in which total BA level increased in comparison to control.After 120 days of the experiment total BA content was similar in the control and quercetin-supplemented samples.	Zhou, Zhang, et al. 2023

Some authors have indicated that the decreased concentration of BA results from the antimicrobial properties of the applied additives (Bozkurt 2006; Cai, Liu, et al. 2015; Es’haghi Gorji et al. 2014; Jia et al. 2020; Lu et al. 2015; Majcherczyk and Surówka 2019; Mannaa, Seo, and Park 2020; Sun et al. 2018; Wang et al. 2021; Wang, Zhang, and Ren 2018; Xu et al. 2022). Based on a recent review of plant antimicrobial agents, disruption of the plasma membrane is the main mechanism of action (Álvarez-Martínez et al. 2021). However, considering the variations in the chemical profiles and structures of plant extracts or EOs, complete clarification of their action remains difficult (Houicher et al. 2021). The main mechanisms underlying the antimicrobial effects of plant additives on BA production are shown in Figure 3. The application of rose polyphenols limited the total bacterial count and simultaneously increased the richness of LAB. Limited growth of other than Lactobacillales microorganisms, namely, Gram-negative bacteria, may be a consequence of the disruption of their quorum sensing activity (Zhang et al. 2017). Polyphenols are a wide group of compounds, and their action largely depends on their structure, that is the number and position of hydroxyl groups, double bonds, and amphipathic characteristics. In addition to an increase in membrane permeability and interaction with the cell wall, the main antibacterial activities of polyphenols include the modulation of cell metabolism through interactions with proteins, including enzymes, and the impact on adenosine triphosphate (ATP) synthesis, inhibition of deoxyribonucleic acid (DNA) and ribonucleic acid (RNA) synthesis, and DNA damage (Houicher et al. 2021; Lobiuc et al. 2023).

Figure 3. Main mechanisms of antimicrobial effects of plant additives on BA production. Created with BioRender.com.

The antimicrobial effects of plant-derived substances can also affect LAB, the growth and activity of which are essential for fermentation. de Souza (2021) summarized the effects of EOs on beneficial microorganisms in food. The author emphasized the scarcity of literature data regarding this issue, as well as the high variability of the effects, which are dependent on the dose and type of EO, type of microorganisms, and food matrix (de Souza 2021).

Based on some previous studies, the inhibitory effect of additives on amino acid decarboxylases is a key factor contributing to the suppression of BA production (Yu et al. 2021; Zhou et al. 2016). Yu et al. (2021) concluded that the reduction in histamine content in fermented sausages was a consequence of the significant suppression of histidine decarboxylase (hdcA) and histidine/histamine antiporter (hdcP) gene expression due to the application of thyme microcapsules. Zhou et al. (2016) indicated that the histamine content limitation in samples supplemented with garlic putatively stems from the unavailability of thiol groups, which are essential for the action of amino acid decarboxylases because of their reaction with allicin. Interestingly, the fermentation of garlic or the addition of garlic to fermented products significantly contributed to an increased content of FAAs and simultaneously limited BA production, which was attributed to the antimicrobial properties of allicin by some researchers (Bahuguna et al. 2019; Świder et al. 2020). The reduced concentrations of putrescine in fermented fish sauce supplemented with star anise may be due to anethole, which could inhibit the activity of the enzymes responsible for putrescine formation, namely, ornithine decarboxylase and agmatine deiminase (Zhou et al. 2016).

Both antimicrobial effects and the suppression of decarboxylase activity are involved in the reduction of BA content in some matrices (Lee et al. 2018; Zhou et al. 2016). Catechins, which exhibit inhibitory effects on the enzymatic activity of decarboxylases, simultaneously remotely affecting bacterial growth, and grapefruit seed extract, which shows antimicrobial properties, have been applied to fermented soybean paste (Lee et al. 2018). The antimicrobial properties of EGCG arise from its direct binding to the peptidoglycan layer and disruption of the cell wall in Gram-positive bacteria. Its inhibitory effect on Gram-negative bacteria results from the oxidative stress induced by the production of hydrogen peroxide (Nikoo, Regenstein, and Ahmadi Gavlighi 2018). In a study by Zhou et al. (2016), histamine and putrescine formation were suppressed mainly through the inhibitory effects of bioactive compounds of plant extracts on enzymes responsible for the formation of these amines, while tyramine concentration was reduced because of the antimicrobial effect of garlic and star anise extracts, as well as ethanol itself. Both the inhibitory effects on the growth of amine-producing bacteria and suppression of spermidine synthase affect the spermidine concentration in fermented fish sauce supplemented with garlic, ginger, or star anise extracts (Zhou et al. 2016). Kongkiattikajorn (2015) emphasized the effect of introducing plant-origin AOs into the product along with additives. The application of ginger extract, in which AO activity was estimated to be ca. 34.3 U/g, resulted in the reduction of the examined BAs after 7 d of Nham fermentation in comparison to the control (85.90%), as well as the initial content (60.44%) (Kongkiattikajorn 2015). In some studies, the synergistic effects of plant-origin additives and starter cultures against BA accumulation were employed, whereby stronger inhibitory activity was exhibited by plant-origin additives in some cases (Lu et al. 2015) and starter cultures in others (Hernández-Macias et al. 2021). Each additive exhibited different activities, which were determined by numerous factors such as the concentration and profile of bioactive compounds present in the additive (or the additive itself when single substances were tested), added dose/quantity, autochthonous and inoculated microorganisms, type of matrix, and applied conditions.

Jia et al. (2020) reported that relatively high concentrations of estragole and trans-anethole in cassia and fennel extracts contributed most to their inhibitory effects on BA formation. The effectiveness of garlic has been attributed to the presence of allicin (Mah, Kim, and Hwang 2009; Zhou et al. 2016), whereas thyme, Thymbra spicata, and Satureja montana EOs have antimicrobial properties through phenolic compounds such as carvacrol and thymol (Bozkurt 2006; Mozuriene et al. 2016; Yu et al. 2021). Owing to their high hydrophobicity, the antimicrobial effect of EOs and their components (for example, thymol and carvacrol) is attributed to the disturbance of the bacterial cell membrane lipid fraction. Damage to membrane integrity results in the leakage of cell contents, such as nucleic acids and proteins (Bouyahya et al. 2019). Epicatechin, epicatechin gallate, epigallocatechin, and EGCG contribute to the wide range of bioactive effects of green tea (Bozkurt 2006). Compounds such as eucalyptol and trans-cinnamaldehyde in cinnamon, eugenol present in anise and clove, and carvacrol, linalool, and α-terpineol in anise were responsible for the antimicrobial properties of the seasoning extracts (Sun et al. 2018). The most abundant substance contributing to the antimicrobial effects of Zataria multiflora Boiss. is carvacrol, which can cross the bacterial cell membrane and increase cell permeability (Bouyahya et al. 2019; Es’haghi Gorji et al. 2014). Capsaicinoids originating from red peppers alter the composition of LAB in kimchi, leading to a decrease in BA content (Kim, Dang, and Ha 2022).

Some attempts to reduce BAs through the use of plant-origin additives have failed. Fortification of sausages with chia or black cumin seeds resulted in significantly increased concentrations of tyramine and putrescine (Borrajo et al. 2021). Application of Nelumbo nucifera (lotus leaves) at 10% concentration enhanced the formation of agmatine, tryptamine, putrescine, histamine, tyramine, spermidine, and spermine in Meju, in comparison to the control and samples supplemented with garlic, Gingko biloba leaves, or a mix of examined additives. Two putative explanations have been proposed by the authors: variability between batches and alteration in the microbial community (Shukla et al. 2018). The addition of cava lees resulted in higher (insignificantly) contents of putrescine, cadaverine, and spermidine in bread, but significantly reduced tyramine and cadaverine concentrations in fermented sausages, indicating that the matrix is a crucial factor affecting the effectiveness of the inhibitory activity of applied additives on BA formation (Hernández-Macias et al. 2021).

Effect of plant-origin additives on sensory properties of fermented products

In addition to the impact on BA content, some of the tested food additives altered the sensory characteristics of the products. Application of grape seed extract prevented deterioration of tarhana color due to increased antioxidative activity (Akan and Ocak 2019), which enhances sausage odor because of the limitation of protein metabolism as well as slower release of thyme EO flavor resulting from the presence of the coating (Yu et al. 2021). Grape seed extract prevented lipid oxidation in smoke-cured bacon, and thus favorably changed the color of the meat product – redness value was increased. The improved lightness of samples supplemented with this additive putatively stemmed from the altered muscle structure due to the different extents of protein denaturation (Wang, Zhang, and Ren 2018). In contrast, the application of Urtica dioica or Hibiscus sabdariffa extracts did not significantly affect the sensory characteristics of dry fermented sausages (Karabacak and Bozkurt 2008). Application of 0.4% Z. multiflora Boiss. reduced BA concentration in cheese the most efficiently, however, obtained product had lower acceptability than products with 0.2 or 0.1% Z. multiflora Boiss. addition (Es’haghi Gorji et al. 2014). The application of 200 or 400 U/g of papain shortened the fermentation time of Chouguiyu from 10 to 7 d with respect to the flavor and taste characteristics of the product, whereby lower levels of the enzyme reduced putrescine and cadaverine content significantly more efficiently (Xu et al. 2022).

Plant additives – economic and environmental aspects

Application of plant-origin food additives represents a prospective direction of sustainable food industry development owing to the superiority of natural food additives over synthetic ones in terms of green policy and health (Zang et al. 2022). Extraction of bioactive compounds from plant wastes is a cost-effective and ecologically friendly way of wasted food management. It is estimated that ca. one-third of the global food production is wasted or lost annually. Apart from huge financial loss (approx. $940 billion per year) it contributes considerably to negative consequences concerning environment i.e., futilely use of fertilizers and fresh water, as well as excessive emission of greenhouse gas (FLW Protocol 2016; Ueda et al. 2022). Currently, the management of generated by-products and waste is one of the major challenges for food and agriculture sector. According to the data collected in some European countries fruit and vegetable waste category represents from ca. 20% (Austria) to 70% (Italy) of total food waste regarding household sector (Esparza et al. 2020). In the whole food chain, plant products constitute 86% (by weight) or 88% (by kcal) of loss and waste food with the following contribution of particular groups: cereals (19 or 53% by weight or by kcal, respectively), roots and tubers (20 or 14%), fruits and vegetables (44 or 13%), oilseeds and pulses (3 or 13%) (World Resources Institute 2019). Reuse of plant origin residues is especially advantageous because their production is one of the largest among all food categories and simultaneously, they are rich source of various bioactive compounds highly appreciated by modern consumers. On the other hand, it is particularly challenging, because of perishable characteristics of this type of products (Esparza et al. 2020). One of the possible ways to valorize plant waste is to use them as substrates in biocatalysis e.g., to produce flavors and aromas (Singh et al. 2023). Different botanical parts of plants, incl. these considered as waste, are rich source of specific substances, such as phenolic compounds, fatty and organic acids, dietary fiber, carotenoids, vitamins, and enzymes, which can be further used for functional food, nutraceuticals, and active packaging development (Baiano 2014; Chamorro et al. 2022). Many of the above mentioned could be used to modify the composition of fermented products to make it more nutritious or to modify fermentation process itself in a desired direction.

Future perspectives

Considering the growing number of people sensitive to BAs (Comas-Basté et al. 2020), as well as increasing interest of consumers in health concerns (de Souza Ribeiro et al. 2022) development of effective, natural, and simple methods for manufacturing low-BA fermented food is an urgent matter. Owing to the complexity of the fermentation process, the development of detailed procedures for each food matrix is essential. The use of plant-based food additives represents a desirable and effective approach to increasing the nutritional value of food products. Optimization of extraction methods should be studied in terms of efficiency and environmental concerns, and attention has been paid to emerging techniques such as Supercritical Carbon Dioxide, Subcritical water, and ultrasound-assisted extraction (Daud et al. 2022). Plant-origin additives intended for application in fermented products must be thoroughly characterized in terms of their chemical composition and standardized with respect to the concentration and stability of the main bioactive molecules. Cutting-edge techniques such as ultra-high-performance liquid/gas chromatography coupled with mass spectrometry can be applied. Chromatography – mass spectrometry and electronic nose, which represent the primary techniques employed to analyze food flavor (Wei et al. 2023), should be used to evaluate sensory attributes, while molecular biology tools, such as metagenomic sequencing, should be used to analyze changes in the microbial community following plant additive application in particular matrices. Methods of bioactive substance application should be precisely analyzed, including the development of new means, such as active packaging, which effectively prevents the accumulation of BAs in meat (Sirocchi et al. 2013), and encapsulation, which is more efficient in reducing histamine content than direct essential oil application (Yu et al. 2021). Regarding economic and ecological concerns, exploring industrial by-products in the search for biologically active compounds is of interest (Banerjee et al. 2017).

Conclusions

Providing fermented foods with reduced BA content remains a significant challenge for food technologists. The entire population benefits from the availability of such products, particularly sensitive individuals. The use of plant-based additives is a promising strategy for this purpose. The different results obtained because of the use of similar additives indicate that the fermentation process is highly complex. Thus, individual additives must be thoroughly examined in target matrices to evaluate their action and prospective effects on BA accumulation. Alterations in the sensory characteristics should also be considered. The effectiveness of applied plant-origin additives depends mainly on the type and dose of the additive, matrix, autochthonous, and inoculated microorganisms, as well as the manufacturing conditions. Antimicrobial features such as destructive action against bacterial cell membranes are the primary mechanisms responsible for the limitation of BAs. The characteristic approach has added value considering its simplicity and relatively low cost, as some bioactive substances can be extracted from byproducts derived from different branches of the food industry. Further studies concerning previously tested and novel plant-origin additives and their combined effects with other BA reduction methods, such as the use of starter cultures, are required.

List of abbreviations
AN	=	Anorexia nervosa
AOs	=	Amine oxidases
ATP	=	Adenosine triphosphate
BAs	=	Biogenic amines
BMI	=	Body Mass Index
CLA	=	Conjugated linoleic acid
DAO	=	Diamine oxidase
DNA	=	Deoxyribonucleic acid
EFSA	=	European Food Safety Authority
EGCG	=	Epigallocatechin gallate
EOs	=	Essential oils
FAAs	=	Free amino acids
GABA	=	γ-aminobutyric acid, gamma aminobutyric acid
GRAS	=	Generally recognized as safe
HDL	=	High-density lipoprotein
HNMT	=	Histamine N-methyltransferase
IBS	=	Irritable bowel syndrome
(IL)-6	=	Interleukin 6
ISAPP	=	International Scientific Association for Probiotics and Prebiotics
LAB	=	Lactic acid bacteria
LDL	=	Low-density lipoprotein
LOAEL	=	Lowest observed adverse effect level
MAOs	=	Monoamine oxidases
MAOIs	=	Monoamine oxidase inhibitors
NOAEL	=	No observed adverse effect level
NSLAB	=	Nonstarter lactic acid bacteria
RNA	=	Ribonucleic acid
SCFAs	=	Short chain fatty acids
TNF-α	=	Tumor necrosis factor
YLD	=	Years lived with disability

Disclosure statement

The authors report there are no competing interests to declare.

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.

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Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.