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Biogenic Amines and Food Safety
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Biogenic Amines and Food Safety

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

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 53195

Printed Edition Available!
A printed edition of this Special Issue is available here.

Special Issue Editors

Prof. Dr. Maria Martuscelli

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Guest Editor
Department of Bioscience and Technology for Food, Agriculture and Environment, University of the Studies of Teramo, via Balzarini 1, 64100 Teramo, Italy
Interests: biogenic amines; food quality; by-products
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Dino Mastrocola

E-Mail Website
Guest Editor
Department of Bioscience and Technology for Food, Agriculture and Environment, University of the Studies of Teramo, via Balzarini 1, 64100 Teramo, Italy
Interests: Maillard reaction products; lipid oxidation; antioxidant activity; enzymatic browning
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The purpose of this Special Issue on “Biogenic amines and food safety” is to focus on biological, technological, and environmental factors affecting the occurrence of biogenic amines (BA) in foods from animal and vegetable origin. The presence of BA in foods is quite frequent and inevitable. BA can be naturally present, derive from the decarboxylation of amino acids by enzymes of microbial origin, or be produced by the transamination of aldehydes by amino acid transaminases. This Special Issue will discuss two aspects of BA in food: 1) BA concentration as a quality index of processes and of raw materials, intermediates, and end products; 2) the risk of creating toxic reactions associated with BA, considering the composition of a whole meal as well as the specific physiological conditions of the consumer. The knowledge of BA levels in foods is important to both consumers and producers, therefore papers discussing the possibility to establish a regulatory system containing food safety criteria for BA, as already existing for histamine in fishery products, are also welcomed.

Prof. Maria Martuscelli
Prof. Dino Mastrocola
Guest Editors

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Keywords

  • biogenic amines
  • food
  • safety
  • quality
  • food process
  • health
  • toxicity
  • pharmacology
  • risk assessment
  • risk management

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Published Papers (12 papers)

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Editorial

Jump to: Research, Review

2 pages, 175 KiB  
Editorial
Biogenic Amines’ Content in Safe and Quality Food
by Maria Martuscelli, Luigi Esposito and Dino Mastrocola
Foods 2021, 10(1), 100; https://doi.org/10.3390/foods10010100 - 6 Jan 2021
Cited by 9 | Viewed by 2546
Abstract
Biogenic amines (BAs) are low-molecular-weight, nitrogenous compounds (mainly polar bases) coming from the decarboxylation of free amino acids or by amination or transamination of aldehydes and ketones [...] Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)

Research

Jump to: Editorial, Review

28 pages, 3639 KiB  
Article
Extensive Chemometric Investigations of Distinctive Patterns and Levels of Biogenic Amines in Fermented Foods: Human Health Implications
by Martin Grootveld, Benita C. Percival and Jie Zhang
Foods 2020, 9(12), 1807; https://doi.org/10.3390/foods9121807 - 5 Dec 2020
Cited by 8 | Viewed by 2677
Abstract
Although biogenic amines (BAs) present in fermented foods exert important health-promoting and physiological function support roles, their excessive ingestion can give rise to deleterious toxicological effects. Therefore, here we have screened the BA contents and supporting food quality indices of a series of [...] Read more.
Although biogenic amines (BAs) present in fermented foods exert important health-promoting and physiological function support roles, their excessive ingestion can give rise to deleterious toxicological effects. Therefore, here we have screened the BA contents and supporting food quality indices of a series of fermented food products using a multianalyte-chemometrics strategy. A liquid chromatographic triple quadrupole mass spectrometric (LC-MS/MS) technique was utilized for the simultaneous multicomponent analysis of 8 different BAs, and titratable acidity, pH, total lipid content, and thiobarbituric acid-reactive substances (TBARS) values were also determined. Rigorous univariate and multivariate (MV) chemometric data analysis strategies were employed to evaluate results acquired. Almost all foods analyzed had individual and total BA contents that were within recommended limits. The chemometrics methods applied were useful for recognizing characteristic patterns of BA analytes and food quality measures between some fermented food classes, and for assessing their inter-relationships and potential metabolic sources. MV analysis of constant sum-normalized BA profile data demonstrated characteristic signatures for cheese (cadaverine only), fermented cod liver oil (2-phenylethylamine, tyramine, and tryptamine), and wine/vinegar products (putrescine, spermidine, and spermine). In conclusion, this LC-MS/MS-linked chemometrics approach was valuable for (1) contrasting and distinguishing BA catabolite signatures between differing fermented foods, and (2) exploring and evaluating the health benefits and/or possible adverse public health risks of such products. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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14 pages, 1300 KiB  
Article
Effect of Brine Concentrations on the Bacteriological and Chemical Quality and Histamine Content of Brined and Dried Milkfish
by Chiu-Chu Hwang, Yi-Chen Lee, Chung-Yung Huang, Hsien-Feng Kung, Hung-Hui Cheng and Yung-Hsiang Tsai
Foods 2020, 9(11), 1597; https://doi.org/10.3390/foods9111597 - 3 Nov 2020
Cited by 7 | Viewed by 3069
Abstract
In this research, the occurrence of hygienic quality and histamine in commercial brined and dried milkfish products, and the effects of brine concentrations on the quality of brined and dried milkfish, were studied. Brined and dried milkfish products (n = 20) collected [...] Read more.
In this research, the occurrence of hygienic quality and histamine in commercial brined and dried milkfish products, and the effects of brine concentrations on the quality of brined and dried milkfish, were studied. Brined and dried milkfish products (n = 20) collected from four retail stores in Taiwan were tested to investigate their histamine-related quality. Among them, five tested samples (25%, 5/20) had histamine contents of more than 5 mg/100 g, the United States Food and Drug Administration guidelines for scombroid fish, while two (10%, 2/20) contained 69 and 301 mg/100 g of histamine, exceeding the 50 mg/100 g potential hazard level. In addition, the effects of brine concentrations (0%, 3%, 6%, 9%, and 15%) on the chemical and bacteriological quality of brined and dried milkfish during sun-drying were evaluated. The results showed that the aerobic plate count (APC), coliform, water activity, total volatile basic nitrogen (TVBN), and histamine content values of the brined and dried milkfish samples decreased with increased brine concentrations, whereas those of salt content and thiobarbituric acid (TBA) increased with increasing brine concentrations. The milkfish samples prepared with 6% NaCl brine had better quality with respect to lower APC, TVBN, TBA, and histamine levels. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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19 pages, 1211 KiB  
Article
Casing Contribution to Proteolytic Changes and Biogenic Amines Content in the Production of an Artisanal Naturally Fermented Dry Sausage
by Annalisa Serio, Jessica Laika, Francesca Maggio, Giampiero Sacchetti, Flavio D’Alessandro, Chiara Rossi, Maria Martuscelli, Clemencia Chaves-López and Antonello Paparella
Foods 2020, 9(9), 1286; https://doi.org/10.3390/foods9091286 - 13 Sep 2020
Cited by 13 | Viewed by 3761
Abstract
The effect of two kinds of casings on the production and characteristics of a dry fermented sausage was investigated. In detail, an Italian product, naturally fermented at low temperatures and normally wrapped in beef casing instead of the most diffused hog one, was [...] Read more.
The effect of two kinds of casings on the production and characteristics of a dry fermented sausage was investigated. In detail, an Italian product, naturally fermented at low temperatures and normally wrapped in beef casing instead of the most diffused hog one, was selected. Two different productions (one traditionally in beef casing (MCB) and another in hog casing (MCH)) were investigated over time to determine the differences particularly regarding proteolytic changes during fermentation and ripening. First of all, the product in hog casing required a longer ripening time, up to 120 days, instead of 45–50 days, because of the lower drying rate, while the microbial dynamics were not significantly modified. Conversely, the proteolysis showed a different evolution, being more pronounced, together with the biogenic amines content up to 341 mg/Kg instead of 265 mg/Kg for the traditional products. The latter products were instead characterized by higher quantities of total free amino acids, 3-methyl butanoic acid, 3-Methyl-1-butanal, and 2-Methylpropanal, enriching the final taste and aroma. The traditional product MCB also showed lower hardness and chewiness than MCH. The results highlight how the choice of casing has a relevant impact on the development of the final characteristics of fermented sausages. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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18 pages, 1470 KiB  
Article
The Role of Enterococcus faecium as a Key Producer and Fermentation Condition as an Influencing Factor in Tyramine Accumulation in Cheonggukjang
by Young Kyoung Park, Young Hun Jin, Jun-Hee Lee, Bo Young Byun, Junsu Lee, KwangCheol Casey Jeong and Jae-Hyung Mah
Foods 2020, 9(7), 915; https://doi.org/10.3390/foods9070915 - 11 Jul 2020
Cited by 20 | Viewed by 3499
Abstract
The study evaluated the role of Enterococcus faecium in tyramine production and its response to fermentation temperature in a traditional Korean fermented soybean paste, Cheonggukjang. Tyramine content was detected in retail Cheonggukjang products at high concentrations exceeding the recommended limit up to [...] Read more.
The study evaluated the role of Enterococcus faecium in tyramine production and its response to fermentation temperature in a traditional Korean fermented soybean paste, Cheonggukjang. Tyramine content was detected in retail Cheonggukjang products at high concentrations exceeding the recommended limit up to a factor of 14. All retail Cheonggukjang products contained Enterococcus spp. at concentrations of at least 6 Log CFU/g. Upon isolation of Enterococcus strains, approximately 93% (157 strains) produced tyramine at over 100 µg/mL. The strains that produced the highest concentrations of tyramine (301.14–315.29 μg/mL) were identified as E. faecium through 16S rRNA sequencing. The results indicate that E. faecium is one of the major contributing factors to high tyramine content in Cheonggukjang. During fermentation, tyramine content in Cheonggukjang groups co-inoculated with E. faecium strains was highest at 45 °C, followed by 37 °C and 25 °C. The tyramine content of most Cheonggukjang groups continually increased as fermentation progressed, except groups fermented at 25 °C. At 45 °C, the tyramine content occasionally exceeded the recommended limit within 3 days of fermentation. The results suggest that lowering fermentation temperature and shortening duration may reduce the tyramine content of Cheonggukjang, thereby reducing the safety risks that may arise when consuming food with high tyramine concentrations. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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20 pages, 701 KiB  
Article
Effect of Fermentation, Drying and Roasting on Biogenic Amines and Other Biocompounds in Colombian Criollo Cocoa Beans and Shells
by Johannes Delgado-Ospina, Carla Daniela Di Mattia, Antonello Paparella, Dino Mastrocola, Maria Martuscelli and Clemencia Chaves-Lopez
Foods 2020, 9(4), 520; https://doi.org/10.3390/foods9040520 - 21 Apr 2020
Cited by 37 | Viewed by 6919
Abstract
The composition of microbiota and the content and pattern of bioactive compounds (biogenic amines, polyphenols, anthocyanins and flavanols), as well as pH, color, antioxidant and reducing properties were investigated in fermented Criollo cocoa beans and shells. The analyses were conducted after fermentation and [...] Read more.
The composition of microbiota and the content and pattern of bioactive compounds (biogenic amines, polyphenols, anthocyanins and flavanols), as well as pH, color, antioxidant and reducing properties were investigated in fermented Criollo cocoa beans and shells. The analyses were conducted after fermentation and drying (T1) and after two thermal roasting processes (T2, 120 °C for 22 min; T3, 135 °C for 15 min). The fermentation and drying practices affected the microbiota of beans and shells, explaining the great variability of biogenic amines (BAs) content. Enterobacteriaceae were counted in a few samples with average values of 103 colony forming units per gram (CFU g−1), mainly in the shell, while Lactobacillus spp. was observed in almost all the samples, with the highest count in the shell with average values of 104 CFU g−1. After T1, the total BAs content was found to be in a range of 4.9÷127.1 mg kg−1DFW; what was remarkable was the presence of cadaverine and histamine, which have not been reported previously in fermented cocoa beans. The total BAs content increased 60% after thermal treatment T2, and of 21% after processing at T3, with a strong correlation (p < 0.05) for histamine (ß = 0.75) and weakly correlated for spermidine (ß = 0.58), spermine (ß = 0.50), cadaverine (ß = 0.47) and serotonine (ß = 0.40). The roasting treatment of T3 caused serotonin degradation (average decrease of 93%) with respect to unroasted samples. However, BAs were detected in a non-alarming concentration (e.g., histamine: n.d ÷ 59.8 mg kg−1DFW; tyramine: n.d. ÷ 26.5 mg kg−1DFW). Change in BAs level was evaluated by principal component analysis. PC1 and PC2 explained 84.9% and 4.5% of data variance, respectively. Antioxidant and reducing properties, polyphenol content and BAs negatively influenced PC1 with both polyphenols and BA increasing during roasting, whereas PC1 was positively influenced by anthocyanins, catechin and epicatechin. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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19 pages, 300 KiB  
Article
Biogenic Amine Contents and Microbial Characteristics of Cambodian Fermented Foods
by Dalin Ly, Sigrid Mayrhofer, Julia-Maria Schmidt, Ulrike Zitz and Konrad J. Domig
Foods 2020, 9(2), 198; https://doi.org/10.3390/foods9020198 - 15 Feb 2020
Cited by 27 | Viewed by 5221
Abstract
Naturally fermented foods are an important part of the typical diet in Cambodia. However, the food safety status of these products has not been widely studied. The aim of this study was, therefore, to provide an overview of the quality of these foods [...] Read more.
Naturally fermented foods are an important part of the typical diet in Cambodia. However, the food safety status of these products has not been widely studied. The aim of this study was, therefore, to provide an overview of the quality of these foods in relation to microbiology and biogenic amines. Additionally, the obtained results were compared to the habits and practices of Cambodians in handling this type of food. A total of 57 fermented foods (42 fishery and 15 vegetable products) were collected from different retail markets in the capital of Cambodia. Pathogenic Salmonella spp., Listeria spp., and Listeria monocytogenes were not detected in 25 g samples. Generally, less than 102 cfu/g of Staphylococcus aureus, Escherichia coli, Pseudomonas spp., Enterobacteriaceae, and molds were present in the fermented foods. Bacillus cereus group members (<102 to 2.3 × 104 cfu/g), lactic acid bacteria (<102 to 1.1 × 107 cfu/g), halophilic and halotolerant bacteria (<102 to 8.9 × 106 cfu/g), sulfite-reducing Clostridium spp. (<102 to 3.5 × 106 cfu/g), and yeasts (<102 to 1.1 × 106 cfu/g) were detected in this study. Still, the presence of pathogenic and spoilage microorganisms in these fermented foods was within the acceptable ranges. Putrescine, cadaverine, tyramine, and histamine were detected in 100%, 89%, 81%, and 75% of the tested products, respectively. The concentrations of histamine (>500 ppm) and tyramine (>600 ppm) were higher than the recommended maximum levels in respectively four and one of 57 fermented foods, which represents a potential health risk. The results suggest that the production process, distribution, and domestic handling of fermented foods should be re-evaluated. Further research is needed for the establishment of applicable preservation techniques in Cambodia. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
13 pages, 1374 KiB  
Article
Effects of Soaking and Fermentation Time on Biogenic Amines Content of Maesil (Prunus Mume) Extract
by So Hee Yoon, Eunmi Koh, Bogyoung Choi and BoKyung Moon
Foods 2019, 8(11), 592; https://doi.org/10.3390/foods8110592 - 19 Nov 2019
Cited by 9 | Viewed by 4099
Abstract
Maesil extract, a fruit-juice concentrate derived from Prunus mume prepared by fermenting with sugar, is widely used with increasing popularity in Korea. Biogenic amines in maesil extract were extracted with 0.4 M perchloric acid, derivatized with dansyl chloride, and detected using high-performance liquid [...] Read more.
Maesil extract, a fruit-juice concentrate derived from Prunus mume prepared by fermenting with sugar, is widely used with increasing popularity in Korea. Biogenic amines in maesil extract were extracted with 0.4 M perchloric acid, derivatized with dansyl chloride, and detected using high-performance liquid chromatography. Among 18 home-made maesil extracts collected from different regions, total biogenic amine content varied from 2.53 to 241.73 mg/L. To elucidate the effects of soaking and fermentation time on biogenic amine content in maesil extract, maesil was soaked in brown sugar for 90 days and the liquid obtained was further fermented for 180 days at 15 and 25 °C, respectively. The main biogenic amines extracted were putrescine and spermidine and the total biogenic amine content was higher at 25 °C than at 15 °C. Soaking at 15 and 25 °C increased the total biogenic amines content from 14.14 to 34.98 mg/L and 37.33 to 69.05 mg/L, respectively, whereas a 180 day fermentation decreased the content from 31.66 to 13.59 mg/L and 116.82 to 57.05 mg/L, respectively. Biogenic amine content was correlated with total amino acid content (particularly, arginine content). Based on these results, we have considered that biogenic amine synthesis can be reduced during maesil extract production by controlling temperature and fermentation time. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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14 pages, 623 KiB  
Article
Modeling Some Possible Handling Ways with Fish Raw Material in Home-Made Sushi Meal Preparation
by Hana Buchtova, Dani Dordevic, Iwona Duda, Alena Honzlova and Piotr Kulawik
Foods 2019, 8(10), 459; https://doi.org/10.3390/foods8100459 - 8 Oct 2019
Cited by 2 | Viewed by 4533
Abstract
The aim of this work was to simulate selected ways of handling with raw fish after its purchase. The experiment was designed as three partial simulations: a) trend in the biogenic amines formation in raw fish caused by breakage of cold chain during [...] Read more.
The aim of this work was to simulate selected ways of handling with raw fish after its purchase. The experiment was designed as three partial simulations: a) trend in the biogenic amines formation in raw fish caused by breakage of cold chain during the transport after purchase, b) the use of a handheld gastronomic unit as an alternative method of smoking fish with cold smoke in the household with regard to a possible increase in polycyclic aromatic hydrocarbon content, and c) whether the cold smoked fish affects selected sensory parameters of nigiri sushi meal prepared by consumers. The material used in the research consisted of: yellowfin tuna (Thunnus albacares) sashimi fillets and the Atlantic salmon (Salmo salar) fillets with skin. The control (fresh/thawed tuna; without interrupting the cold chain) and experimental (fresh/thawed tuna; cold chain was interrupted by incubation at 35 °C/6 h) samples were stored at 2 ± 2 °C for 8 days and analyzed after 1st, 4th and 8th day of the cold storage. Histamine content was very low throughout the experiment, though one exception was found (thawed tuna without interrupting the cold chain: 272.05 ± 217.83 mg·kg−1/8th day). Tuna samples contained more PAH (4.22 µg·kg−1) than salmon samples (1.74 µg·kg−1). Alarming increases of benzo(a)anthracene (1.84 μg·k−1) and chrysene (1.10 μg·kg−1) contents in smoked tuna were detected. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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14 pages, 1858 KiB  
Article
Identification of a Lactic Acid Bacteria to Degrade Biogenic Amines in Chinese Rice Wine and Its Enzymatic Mechanism
by Tianjiao Niu, Xing Li, Yongjie Guo and Ying Ma
Foods 2019, 8(8), 312; https://doi.org/10.3390/foods8080312 - 2 Aug 2019
Cited by 33 | Viewed by 5075
Abstract
A L. plantarum, CAU 3823, which can degrade 40% of biogenic amines (BAs) content in Chinese rice wine (CRW) at the end of post-fermentation, was selected and characterized in this work. It would be an optimal choice to add 106 cfu/mL [...] Read more.
A L. plantarum, CAU 3823, which can degrade 40% of biogenic amines (BAs) content in Chinese rice wine (CRW) at the end of post-fermentation, was selected and characterized in this work. It would be an optimal choice to add 106 cfu/mL of selected strain into the fermentation broth to decrease the BAs while keeping the character and quality of CRW. Nine amine oxidases were identified from the strain and separated using Sephadex column followed by LC-MS/MS analysis. The purified amine oxidase mixture showed a high monoamine oxidase activity of 19.8 U/mg, and more than 40% of BAs could be degraded. The biochemical characters of the amine oxidases were also studied. This work seeks to provide a better solution to degrade BAs in CRW prior to keeping the character and quality of CRW and a better understanding of the degradability of the strain to the BAs. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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19 pages, 709 KiB  
Article
Biogenic Amines, Phenolic, and Aroma-Related Compounds of Unroasted and Roasted Cocoa Beans with Different Origin
by Umile Gianfranco Spizzirri, Francesca Ieri, Margherita Campo, Donatella Paolino, Donatella Restuccia and Annalisa Romani
Foods 2019, 8(8), 306; https://doi.org/10.3390/foods8080306 - 1 Aug 2019
Cited by 24 | Viewed by 4102
Abstract
Biogenic amines (BAs), polyphenols, and aroma compounds were determined by chromatographic techniques in cocoa beans of different geographical origin, also considering the effect of roasting (95, 110, and 125 °C). In all samples, methylxantines (2.22–12.3 mg kg−1) were the most abundant [...] Read more.
Biogenic amines (BAs), polyphenols, and aroma compounds were determined by chromatographic techniques in cocoa beans of different geographical origin, also considering the effect of roasting (95, 110, and 125 °C). In all samples, methylxantines (2.22–12.3 mg kg−1) were the most abundant followed by procyanidins (0.69–9.39 mg kg−1) and epicatechin (0.16–3.12 mg kg−1), all reduced by heat treatments. Volatile organic compounds and BAs showed variable levels and distributions. Although showing the highest BAs total content (28.8 mg kg−1), Criollo variety presented a good aroma profile, suggesting a possible processing without roasting. Heat treatments influenced the aroma compounds especially for Nicaragua sample, increasing more than two-fold desirable aldehydes and pyrazines formed during the Maillard cascade and the Strecker degradation. As the temperature increased, the concentration of BAs already present in raw samples increased as well, although never reaching hazardous levels. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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Review

Jump to: Editorial, Research

15 pages, 672 KiB  
Review
Occurrence and Reduction of Biogenic Amines in Kimchi and Korean Fermented Seafood Products
by Young Kyoung Park, Jae Hoan Lee and Jae-Hyung Mah
Foods 2019, 8(11), 547; https://doi.org/10.3390/foods8110547 - 4 Nov 2019
Cited by 33 | Viewed by 6118
Abstract
Biogenic amines produced during fermentation may be harmful when ingested in high concentrations. As current regulations remain insufficient to ensure the safety of fermented vegetable products, the current study determined the risks associated with the consumption of kimchi by evaluating the biogenic amine [...] Read more.
Biogenic amines produced during fermentation may be harmful when ingested in high concentrations. As current regulations remain insufficient to ensure the safety of fermented vegetable products, the current study determined the risks associated with the consumption of kimchi by evaluating the biogenic amine concentrations reported by various studies. Upon evaluation, some kimchi products were found to contain histamine and tyramine at potentially hazardous concentrations exceeding the recommended limit of 100 mg/kg for both histamine and tyramine. The biogenic amines may have originated primarily from metabolic activity by microorganisms during fermentation, as well as from Jeotgal (Korean fermented seafood) and Aekjeot (Korean fermented fish sauce) products commonly used as ingredients for kimchi production. Many studies have suggested that Jeotgal and Aekjeot may contribute to the histamine and tyramine content in kimchi. Microorganisms isolated from kimchi and Jeotgal have been reported to produce both histamine and tyramine. Despite the potential toxicological risks, limited research has been conducted on reducing the biogenic amine content of kimchi and Jeotgal products. The regulation and active monitoring of biogenic amine content during kimchi production appear to be necessary to ensure the safety of the fermented vegetable products. Full article
(This article belongs to the Special Issue Biogenic Amines and Food Safety)
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