Special Issue "Biogenic Amines on Food Safety"

A special issue of Foods (ISSN 2304-8158). This special issue belongs to the section "Food Physics and (Bio)Chemistry".

Deadline for manuscript submissions: closed (25 October 2018)

Special Issue Editors

Guest Editor
Dr. Claudia Ruiz-Capillas

Senior Research Scientist, Department of Products (DPRD), Group on Meat and Meat Products (CARPROCAR), Instituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain
Website | E-Mail
Interests: biogenic amines; food safety; quality indices; functional and healthy food; meat and meat products; fish and fish products; flow injection analysis; additives
Guest Editor
Dr. Ana Herrero Herranz

Departamento de Productos, Instituto de Ciencia y Tecnología de Alimentos y Nutrición (CSIC), José Antonio Novais, 10, 28040-Madrid, Spain
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Phone: (+34)-91-549-23-00 (Ext. 231331)
Fax: (+34)-91-549-36-27
Interests: Raman spectroscopy; infrared spectroscopy; development of healthy meat products; biogenic amines; food safety; quality indices

Special Issue Information

Dear Colleagues,

Biogenic amines have been known for some time. These compounds are found in varying concentrations in a wide range of foods (fish, cheese, meat, wine, beer, vegetables, etc.) and their formations are influenced by different factors associated to those foods (composition, additives, ingredients, storage, microorganism, packaging, handing, conservation, etc.). The intake of foods containing high concentrations of biogenic amines can present a health hazard. Additionally, they may have been used to establish indexes in various foods in order to signal the degree of freshness and/or deterioration of food. Nowadays, there has been an increase in the number of food poisoning episodes in consumers associated with the presence of these biogenic amines in food, mainly associated with histamines. Food safety is one of the main concerns of the consumer and safety agencies of different countries (EFSA, FDA, FSCJ, etc.), which have, as one of their main objectives, to control these biogenic amines, principally histamine, to assure a high level of food safety.

Therefore, it is necessary to deepen our understanding of the formation, monitoring and reduction of biogenic amines during the development, processing and storage of food, even the effect of biogenic amines in consumers after digestion of foods with different levels of these compounds.

With this aim, we are preparing a Special Issue on the topic of "Biogenic Amines in Food Safety", and we invite researchers to contribute original and unpublished research articles and reviews articles that involve studies of biogenic amines in food, which can provide an update to our knowledge of these compunds and their impacts on food quality and food safety.

Dr. Claudia Ruiz-Capillas
Dr. Ana Herrero Herranz
Guest Editors

Manuscript Submission Information

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Keywords

  • Biogenic amines
  • Foods
  • Food Safety
  • Histamine poisoning
  • Quality index
  • Tyramine
  • Health
  • Toxicological aspects
  • Digestion Food
  • Immune System
  • Biogenic amines analysis
  • Intake foods
  • Processing
  • Storage
  • Microorganisms

Published Papers (11 papers)

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Research

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Open AccessArticle The Occurrence of Biogenic Amines and Determination of Biogenic Amine-Producing Lactic Acid Bacteria in Kkakdugi and Chonggak Kimchi
Received: 3 February 2019 / Revised: 8 February 2019 / Accepted: 12 February 2019 / Published: 14 February 2019
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Abstract
In this study, biogenic amine content in two types of fermented radish kimchi (Kkakdugi and Chonggak kimchi) was determined by high performance liquid chromatography (HPLC). While most samples had low levels of biogenic amines, some samples contained histamine content over the toxicity [...] Read more.
In this study, biogenic amine content in two types of fermented radish kimchi (Kkakdugi and Chonggak kimchi) was determined by high performance liquid chromatography (HPLC). While most samples had low levels of biogenic amines, some samples contained histamine content over the toxicity limit. Additionally, significant amounts of total biogenic amines were detected in certain samples due to high levels of putrefactive amines. As one of the significant factors influencing biogenic amine content in both radish kimchi, Myeolchi-aekjoet appeared to be important source of histamine. Besides, tyramine-producing strains of lactic acid bacteria existed in both radish kimchi. Through 16s rRNA sequencing analysis, the dominant species of tyramine-producing strains was identified as Lactobacillus brevis, which suggests that the species is responsible for tyramine formation in both radish kimchi. During fermentation, a higher tyramine accumulation was observed in both radish kimchi when L. brevis strains were used as inocula. The addition of Myeolchi-aekjeot affected the initial concentrations of histamine and cadaverine in both radish kimchi. Therefore, this study suggests that reducing the ratio of Myeolchi-aekjeot to other ingredients (and/or using Myeolchi-aekjeot with low biogenic amine content) and using starter cultures with ability to degrade and/or inability to produce biogenic amines would be effective in reducing biogenic amine content in Kkakdugi and Chonggak kimchi. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Open AccessArticle The Determination of Some Microbiological and Chemical Features in Herby Cheese
Received: 7 December 2018 / Revised: 25 December 2018 / Accepted: 7 January 2019 / Published: 11 January 2019
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Abstract
The objective of this study is to measure the amounts of biogenic amines, microbial counts, values of pH, titratable acidity, dry matter, and salt (%) in herby cheese, a very popular staple in the Turkish diet, and to evaluate the concentration of biogenic [...] Read more.
The objective of this study is to measure the amounts of biogenic amines, microbial counts, values of pH, titratable acidity, dry matter, and salt (%) in herby cheese, a very popular staple in the Turkish diet, and to evaluate the concentration of biogenic amines in terms of public health risks. A high-performance liquid chromatography (HPLC) method was used for the determination of eight biogenic amines in 100 herby cheeses sold in the local markets of Van. The bacterial load of the herby cheeses ranged between 4.0 and 8.90 log CFU/g for viable total aerobic mesophilic bacteria (TAMB), <1 and 7.0 log CFU/g for lactic bacteria (LAB), <1 and 6.08 log CFU/g for coliform bacteria, <1 and 5.81 log CFU/g for Enterobacteriaceae, <1 and 2.60 log CFU/g for Staphylococcus aureus, and 3.70 and 8.05 log CFU/g for yeasts and molds. The results obtained suggested significant changes in the pH, titratable acidity, dry matter, and salt contents of the examined herby cheese samples. The detection levels of biogenic amines in the samples ranged from <0.025 to 33.36 mg/kg for tryptamine, from <0.038 to 404.57 mg/kg for β-phenylethylamine, from 0.03 to 426.35 mg/kg for putrescine, from <0.039 to 1438.22 mg/kg for cadaverine, from <0.033 to 469 mg/kg for histamine, from <0.309 to 725.21 mg/kg for tyramine, from <0.114 to 1.70 mg/kg for spermidine, and from <0.109 to 1.88 mg/kg for spermine. As a result, these cheeses are fit for consumption in terms of the amounts of biogenic amines they contain. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
Open AccessArticle Screening Method to Evaluate Amino Acid-Decarboxylase Activity of Bacteria Present in Spanish Artisanal Ripened Cheeses
Foods 2018, 7(11), 182; https://doi.org/10.3390/foods7110182
Received: 13 September 2018 / Revised: 22 October 2018 / Accepted: 31 October 2018 / Published: 6 November 2018
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Abstract
A qualitative microplate screening method, using both low nitrogen (LND) and low glucose (LGD) decarboxylase broths, was used to evaluate the biogenic amine (BA) forming capacity of bacteria present in two types of Spanish ripened cheeses, some of them treated by high hydrostatic [...] Read more.
A qualitative microplate screening method, using both low nitrogen (LND) and low glucose (LGD) decarboxylase broths, was used to evaluate the biogenic amine (BA) forming capacity of bacteria present in two types of Spanish ripened cheeses, some of them treated by high hydrostatic pressure. BA formation in decarboxylase broths was later confirmed by High Performance Liquid Chromatography (HPLC). An optimal cut off between 10–25 mg/L with a sensitivity of 84% and a specificity of 92% was obtained when detecting putrescine (PU), tyramine (TY) and cadaverine (CA) formation capability, although these broths showed less capacity detecting histamine forming bacteria. TY forming bacteria were the most frequent among the isolated BA forming strains showing a strong production capability (exceeding 100 mg/L), followed by CA and PU formers. Lactococcus, Lactobacillus, Enterococcus and Leuconostoc groups were found as the main TY producers, and some strains were also able to produce diamines at a level above 100 mg/L, and probably ruled the BA formation during ripening. Enterobacteriaceae and Staphylococcus spp., as well as some Bacillus spp. were also identified among the BA forming bacteria isolated. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Open AccessArticle High Hydrostatic Pressure as a Tool to Reduce Formation of Biogenic Amines in Artisanal Spanish Cheeses
Received: 28 July 2018 / Revised: 24 August 2018 / Accepted: 24 August 2018 / Published: 30 August 2018
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Abstract
Two artisanal varieties of cheese made in Spain, one made of ewes’ raw milk and the other of goats’ raw milk were selected to evaluate the effect of a high hydrostatic pressure (HHP) treatment at 400 MPa during 10 min at 2 °C [...] Read more.
Two artisanal varieties of cheese made in Spain, one made of ewes’ raw milk and the other of goats’ raw milk were selected to evaluate the effect of a high hydrostatic pressure (HHP) treatment at 400 MPa during 10 min at 2 °C on the formation of biogenic amines (BA). These conditions were applied at the beginning of the ripening (before the 5th day; HHP1) and in the case of ewes’ milk cheeses also after 15th days (HHP15). BA formation was greatly influenced by HHP treatments in both types of cheese. HHP1 treatments significantly reduced the amounts of BA after ripening, being tyramine and putrescine the most affected BA in goats’ milk cheeses and tyramine and cadaverine in ewes’ milk cheeses. The BA reduction in the HHP1 samples could be explained by the significant decrease in microbiological counts, especially in the LAB, enteroccocci and enterobacteria groups at the beginning of ripening. The proteolysis in these samples was also affected reducing the amount of free amino acids. Although proteolysis in ewes’ milk cheeses HHP15 was similar than in control samples a reduction of BA was observed probably because the decrease caused on microbial counts. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
Open AccessArticle Quality Assessment of Fresh Meat from Several Species Based on Free Amino Acid and Biogenic Amine Contents during Chilled Storage
Received: 19 July 2018 / Revised: 21 August 2018 / Accepted: 23 August 2018 / Published: 25 August 2018
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Abstract
This paper studies the changes that occur in free amino acid and biogenic amine contents of raw meats (beef, pork, lamb, chicken and turkey) during storage (2 °C, 10 days). The meat cuts samples were harvested from a retail outlet (without getting information [...] Read more.
This paper studies the changes that occur in free amino acid and biogenic amine contents of raw meats (beef, pork, lamb, chicken and turkey) during storage (2 °C, 10 days). The meat cuts samples were harvested from a retail outlet (without getting information on the animals involved) as the following: Beef leg (four muscles), pork leg (five muscles), lamb leg (seven muscles), turkey leg (four muscles), and chicken breast (one muscle). Meat composition varied according to meat types. In general, pH, microbiology counts, biogenic amine (BA), and free amino acid (FAA) contents were also affected by meat types and storage time (p < 0.05). Chicken and turkey presented the highest levels (p < 0.05) of FAAs. Total free amino acids (TFAA) were higher (p < 0.05) in white meats than in red ones. The behavior pattern, of the total free amino acids precursors (TFAAP) of Bas, was saw-toothed, mainly in chicken and turkey meat during storage, which limits their use as quality indexes. Spermidine and spermine contents were initially different among the meats. Putrescine was the most prevalent BA (p < 0.05) irrespective of species. In general, chicken and turkey contained the highest (p < 0.05) levels of BAs, and TFAAP of BAs. In terms of the biogenic amine index (BAI), the quality of chicken was the worst while beef meat was the only sample whose quality remained acceptable through the study. This BAI seems to be more suitable as a quality index for white meat freshness than for red meat, especially for beef. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Open AccessArticle Influence of Iodine Feeding on Microbiological and Physico-Chemical Characteristics and Biogenic Amines Content in a Raw Ewes’ Milk Cheese
Received: 27 May 2018 / Revised: 23 June 2018 / Accepted: 6 July 2018 / Published: 7 July 2018
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Abstract
Iodine is an essential trace element involved in the regulation of thyroid metabolism and antioxidant status in humans and animals. The aim of this study was to evaluate the effect of ewes’ dietary iodine supplementation on biogenic amines content as well as microbiological [...] Read more.
Iodine is an essential trace element involved in the regulation of thyroid metabolism and antioxidant status in humans and animals. The aim of this study was to evaluate the effect of ewes’ dietary iodine supplementation on biogenic amines content as well as microbiological and physico-chemical characteristics in a raw milk cheese at different ripening times (milk, curd, and 2, 7, 15, 30, 60, and 90 days). Two cheese-making trials were carried out using milk from ewes fed with unifeed (Cheese A) or with the same concentrate enriched with iodine (Cheese B). The results indicated that the counts of principal microbial groups and physico-chemical characteristics were quite similar in both cheeses at day 90. Cheese B was characterized by a higher content of biogenic amines and propionic acid. Propionic bacteria were found in both cheeses mainly in Trial B in agreement with the higher content of propionic acid detected. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Review

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Open AccessFeature PaperReview Bacterial Production and Control of Biogenic Amines in Asian Fermented Soybean Foods
Received: 27 January 2019 / Revised: 14 February 2019 / Accepted: 19 February 2019 / Published: 25 February 2019
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Abstract
Fermented soybean foods possess significant health-promoting effects and are consumed worldwide, especially within Asia, but less attention has been paid to the safety of the foods. Since fermented soybean foods contain abundant amino acids and biogenic amine-producing microorganisms, it is necessary to understand [...] Read more.
Fermented soybean foods possess significant health-promoting effects and are consumed worldwide, especially within Asia, but less attention has been paid to the safety of the foods. Since fermented soybean foods contain abundant amino acids and biogenic amine-producing microorganisms, it is necessary to understand the presence of biogenic amines in the foods. The amounts of biogenic amines in most products have been reported to be within safe levels. Conversely, certain products contain vasoactive biogenic amines greater than toxic levels. Nonetheless, government legislation regulating biogenic amines in fermented soybean foods is not found throughout the world. Therefore, it is necessary to provide strategies to reduce biogenic amine formation in the foods. Alongside numerous existing intervention methods, the use of Bacillus starter cultures capable of degrading and/or incapable of producing biogenic amines has been proposed as a guaranteed way to reduce biogenic amines in fermented soybean foods, considering that Bacillus species have been known as fermenting microorganisms responsible for biogenic amine formation in the foods. Molecular genetic studies of Bacillus genes involved in the formation and degradation of biogenic amines would be helpful in selecting starter cultures. This review summarizes the presence and control strategies of biogenic amines in fermented soybean foods. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Open AccessReview Impact of Biogenic Amines on Food Quality and Safety
Received: 20 December 2018 / Revised: 30 January 2019 / Accepted: 5 February 2019 / Published: 8 February 2019
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Abstract
Today, food safety and quality are some of the main concerns of consumer and health agencies around the world. Our current lifestyle and market globalization have led to an increase in the number of people affected by food poisoning. Foodborne illness and food [...] Read more.
Today, food safety and quality are some of the main concerns of consumer and health agencies around the world. Our current lifestyle and market globalization have led to an increase in the number of people affected by food poisoning. Foodborne illness and food poisoning have different origins (bacteria, virus, parasites, mold, contaminants, etc.), and some cases of food poisoning can be traced back to chemical and natural toxins. One of the toxins targeted by the Food and Drug Administration (FDA) and European Food Safety Authority (EFSA) is the biogenic amine histamine. Biogenic amines (BAs) in food constitute a potential public health concern due to their physiological and toxicological effects. The consumption of foods containing high concentrations of biogenic amines has been associated with health hazards. In recent years there has been an increase in the number of food poisoning cases associated with BAs in food, mainly in relation to histamines in fish. We need to gain a better understanding of the origin of foodborne disease and how to control it if we expect to keep people from getting ill. Biogenic amines are found in varying concentrations in a wide range of foods (fish, cheese, meat, wine, beer, vegetables, etc.), and BA formation is influenced by different factors associated with the raw material making up food products, microorganisms, processing, and conservation conditions. Moreover, BAs are thermostable. Biogenic amines also play an important role as indicators of food quality and/or acceptability. Hence, BAs need to be controlled in order to ensure high levels of food quality and safety. All of these aspects will be addressed in this review. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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Open AccessReview Biogenic Amine Production by Lactic Acid Bacteria: A Review
Received: 26 November 2018 / Revised: 18 December 2018 / Accepted: 2 January 2019 / Published: 7 January 2019
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Abstract
Lactic acid bacteria (LAB) are considered as the main biogenic amine (BA) producers in fermented foods. These compounds derive from amino acid decarboxylation through microbial activities and can cause toxic effects on humans, with symptoms (headache, heart palpitations, vomiting, diarrhea) depending also on [...] Read more.
Lactic acid bacteria (LAB) are considered as the main biogenic amine (BA) producers in fermented foods. These compounds derive from amino acid decarboxylation through microbial activities and can cause toxic effects on humans, with symptoms (headache, heart palpitations, vomiting, diarrhea) depending also on individual sensitivity. Many studies have focused on the aminobiogenic potential of LAB associated with fermented foods, taking into consideration the conditions affecting BA accumulation and enzymes/genes involved in the biosynthetic mechanisms. This review describes in detail the different LAB (used as starter cultures to improve technological and sensorial properties, as well as those naturally occurring during ripening or in spontaneous fermentations) able to produce BAs in model or in real systems. The groups considered were enterococci, lactobacilli, streptococci, lactococci, pediococci, oenococci and, as minor producers, LAB belonging to Leuconostoc and Weissella genus. A deeper knowledge of this issue is important because decarboxylase activities are often related to strains rather than to species or genera. Moreover, this information can help to improve the selection of strains for further applications as starter or bioprotective cultures, in order to obtain high quality foods with reduced BA content. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
Open AccessReview Biogenic Amines in Plant-Origin Foods: Are they Frequently Underestimated in Low-Histamine Diets?
Foods 2018, 7(12), 205; https://doi.org/10.3390/foods7120205
Received: 8 November 2018 / Revised: 5 December 2018 / Accepted: 12 December 2018 / Published: 14 December 2018
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Abstract
Low-histamine diets are currently used to reduce symptoms of histamine intolerance, a disorder in histamine homeostasis that increases plasma levels, mainly due to reduced diamine-oxidase (DAO) activity. These diets exclude foods, many of them of plant origin, which patients associate with the onset [...] Read more.
Low-histamine diets are currently used to reduce symptoms of histamine intolerance, a disorder in histamine homeostasis that increases plasma levels, mainly due to reduced diamine-oxidase (DAO) activity. These diets exclude foods, many of them of plant origin, which patients associate with the onset of the symptomatology. This study aimed to review the existing data on histamine and other biogenic amine contents in nonfermented plant-origin foods, as well as on their origin and evolution during the storage or culinary process. The only plant-origin products with significant levels of histamine were eggplant, spinach, tomato, and avocado, each showing a great variability in content. Putrescine has been found in practically all plant-origin foods, probably due to its physiological origin. The high contents of putrescine in certain products could also be related to the triggering of the symptomatology by enzymatic competition with histamine. Additionally, high spermidine contents found in some foods should also be taken into account in these diets, because it can also be metabolized by DAO, albeit with a lower affinity. It is recommended to consume plant-origin foods that are boiled or are of maximum freshness to reduce biogenic amine intake. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
Open AccessReview What We Know and What We Need to Know about Aromatic and Cationic Biogenic Amines in the Gastrointestinal Tract
Received: 1 August 2018 / Revised: 22 August 2018 / Accepted: 29 August 2018 / Published: 4 September 2018
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Abstract
Biogenic amines derived from basic and aromatic amino acids (B/A-BAs), polyamines, histamine, serotonin, and catecholamines are a group of molecules playing essential roles in many relevant physiological processes, including cell proliferation, immune response, nutrition and reproduction. All these physiological effects involve a variety [...] Read more.
Biogenic amines derived from basic and aromatic amino acids (B/A-BAs), polyamines, histamine, serotonin, and catecholamines are a group of molecules playing essential roles in many relevant physiological processes, including cell proliferation, immune response, nutrition and reproduction. All these physiological effects involve a variety of tissue-specific cellular receptors and signalling pathways, which conforms to a very complex network that is not yet well-characterized. Strong evidence has proved the importance of this group of molecules in the gastrointestinal context, also playing roles in several pathologies. This work is based on the hypothesis that integration of biomedical information helps to reach new translational actions. Thus, the major aim of this work is to combine scientific knowledge on biomolecules, metabolism and physiology of the main B/A-BAs involved in the pathophysiology of the gastrointestinal tract, in order to point out important gaps in information and other facts deserving further research efforts in order to connect molecular information with pathophysiological observations. Full article
(This article belongs to the Special Issue Biogenic Amines on Food Safety)
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