Formation Of Biogenic Amines Research Articles

Effects of specific lactic acid bacteria species on biogenic amine production by foodborne pathogen

SummaryThe influences of lactic acid bacteria (LAB) on biogenic amines formation by foodborne pathogens (FBP) were investigated. Biogenic amines production by single and mix cultures was tested in histidine decarboxylase broth. All of the mix cultures (LAB with FBP) inhibited significantly (P < 0.05) the ammonia accumulation except for Escherichia coli with Lactococcus lactic subsp. lactic and Lactobacillus plantarum. Although LAB with most of the pathogen showed considerably stimulation effects on putrescine, cadaverine, spermine, 2‐phenylethylamine, histamine (HIS), tyramine, trimethylamine, dopamine and agmatine (AGM), some of the LAB with pathogens showed poor inhibition effect on different amines formation. HIS production by Klebiella pneumonia was 0.16 mg L−1, whereas HIS value in presence of Lb. plantarum increased to 30.92 mg L−1. Consequently, LAB inhibition of the ammonium production by FBP is favourable, while the stimulation effects of LAB on biogenic amines formation by FBPs are not desirable for food industry.

Effects of rosemary and sage tea extract on biogenic amines formation of sardine (Sardina pilchardus) fillets

SummaryNatural antimicrobials and antioxidants from rosemary (Rosmarinus officinalis) and sage tea (Salvia officinalis) were produced using solvent extraction method. The effect of two extracts on ammonia (AMN) and biogenic amines (BAs) formation in vacuum packed sardine (Sardina pilchardus) fillets stored at 3 ± 1 °C was investigated for 20 days. Although the effect of extracts was dependent on specific amine and storage time, phenolic compounds from rosemary and sage tea generally resulted in lower AMN and BAs accumulation in sardine muscle. Putrescine (PUT) and cadaverine (CAD) were the most abundant amines, while histamine (HIS) concentration ranged from 2.05 to 28.77 mg 100g−1. Rosemary and sage tea extracts significantly reduced HIS, PUT, CAD and trimethylamine accumulation in the fish muscle (P < 0.05) while stimulating effect of extracts was observed on serotonin and agmatine formation. At the end of the storage period, PUT and CAD contents of control were 100‐fold higher than those of treated groups.

Binding to extracellular matrix proteins and formation of biogenic amines by food-associated coagulase-negative staphylococci

In connection with a study on the DNA microarray based detection of genes involved in safety and technologically relevant properties ( Seitter (née Resch) et al., 2011), food-associated coagulase-negative staphylococci (CNS) were investigated phenotypically with regard to their ability to bind to the extracellular matrix proteins (ECM) and to produce biogenic amines. The properties have been shown to be involved in the colonization of injured tissue and invasion into host cells as well as in pharmacologic effects on humans, respectively. The CNS exhibited a low, but nevertheless clearly measurable ECM binding capacity, except for strains of Staphylococcus equorum and Staphylococcus succinus, which show a comparable or even higher binding to fibrinogen and fibronectin than that of the control strain Staphylococcus aureus Cowan. Formation of biogenic amines could be often detected in S. carnosus, S. condimenti and S. strains, but rarely in S. equorum and not in S. succinus and S. xylosus strains. Mostly, 2-phenylethylamine, tyramine and tryptamine were formed by resting cells in amounts < 25 mg/l, whereas growing cells formed high amounts (> 100 mg/l) of 2-phenylethylamine and putrescine. This study confirmed the need of consideration of ECM binding and biogenic amine formation in the safety assessment of CNS used in the production of fermented foods.

DNA microarray based detection of genes involved in safety and technologically relevant properties of food associated coagulase-negative staphylococci

Aim of the work was to design a polynucleotide based DNA microarray as screening tool to detect genes in food associated coagulase-negative staphylococci (CNS). A focus was laid on genes with potential health concern and technological relevance. The microarray contained 220 probes for genes encoding antibiotic resistances, hemolysins, toxins, amino acid decarboxylases (e.g. biogenic amine formation), binding proteins to extracellular matrix (ECM), lipases, proteases, stress response factors, or nitrate dissimilation. Hybridization of genomic DNA isolated from 32 phenotypically characterized CNS permitted to detect numerous genes, corresponding with the phenotype. However, numerous hybridization signals were obtained for genes without any detectable phenotype. The antibiotic resistance genes blaZ, lnuA, and tetK involved in ß-lactam, lincomycin and tetracycline resistance, respectively, were rarely identified in CNS, however, all species contained some strains with such resistance genes. Decarboxylase genes involved in biogenic amine formation were detected regularly in Staphylococcus carnosus, S. condimenti, S. piscifermentans and S. equorum, but was rarely correlated with the phenotype. The same applied for the fibrinogen ( clf) and fibronectin ( fbp) binding protein genes, whose phenotype (binding assay) was only correlated in S. equorum and Staphylococcus succinus. Although some CNS showed hemolytic activity and enterotoxin production (Immunoblot) the corresponding genes could not be verified. Technological relevant genes such as proteases or lipases revealed good hybridization signals. In addition, genes involved in nitrate dissimilation ( nre, nar, nir), catalase ( kat), or superoxide dismutase ( sod) were well detected. Interestingly, genes involved in dissimilatory nitrate reduction were more prevalent in strains of S. carnosus, S. condimenti and S. piscifermentans than of S. equorum, S. succinus and S. xylosus.

Formation of biogenic amines in fillets and minced flesh of three freshwater fish species stored at 3 °C and 15 °C

The aim of the present study was to compare the dynamics of biogenic amines formation in three freshwater fish species, to compare the progress of chemical changes in filleted and minced flesh, to find correlations of such changes with sensory properties and to find possible quality indicators for selected fish species. Samples (n = 156) of fish fillets and fish mince of common carp (Cyprinus carpio), rainbow trout (Oncorhynchus mykiss) and perch (Perca fluviatilis) were stored at 3 °C and 15 °C. The amines were determined as the N-substituted benzamides, after derivatization with benzoylchloride by micellar electrokinetic capillary chromatography. Based on the biogenic amine contents and sensory properties, the shelf life of samples at 3 °C was 11–16 days and 7–10 days for fillets and mince, respectively, and 2–3 days at 15 °C regardless of sample processing. Content of putrescine seems to be a good quality indicator for all examined fish species. The fish species and the method of flesh processing did not have a significant influence on the putrescine formation. Tyramine was formed mainly in carp and trout mince at 15 °C. Samples of good and acceptable quality did not contain toxicologically significant concentrations of histamine or tyramine. Contrary to marine fish, information about biogenic amines contents in freshwater fish is scarce. Comparison of the dynamics of amines formation in fillets and processed fish flesh has not been studied yet. The progress of decomposition processes is compared based on dynamic models.

Effect of γ-irradiation upon biogenic amine formation in blue cheese during storage

The evolution in biogenic amine content of 12-day old Blue cheese, was monitored throughout storage at 5 °C, either non-irradiated or γ-irradiated at 2, 4 or 6 kGy. On a dry weight (DW) basis, the total content of biogenic amines increased from 1023.4 to 2310.2 mg kg DW −1 in non-irradiated cheeses within 90 d, but decreased from 976.7 to 431.5 mg kg DW −1 after irradiation at 6 kGy. Tyramine was dominant; it accounted for 96.1% of the total in non-irradiated cheeses, and 92.8–94.3% in their irradiated counterparts by 90 d of storage. From 35.7 mg kg DW −1 in 90 d non-irradiated cheese, histamine decreased to 29.0 mg kg DW −1 following irradiation at 2 kGy, and was not detected at 4–6 kGy. In sensory terms, irradiated cheeses were fully comparable with non-irradiated ones, except at the highest level of irradiation and longest storage times. Irradiation thus proved effective and useful in controlling biogenic amine levels in Blue cheese during storage.

Biogenic amines formation in Atlantic bonito (Sarda sarda) fillets packaged with modified atmosphere and vacuum, wrapped in chitosan and cling film at 4 °C

A study was carried out to determine the effect of vacuum packed (VP) and modified atmosphere (MAP) (100% CO2) packing, chitosan film and cling film (CF) wrapping on the formation of biogenic amines and trimethylamine (TMA) during storage of Atlantic bonito (Sarda sarda) fillets at 4 °C. The biogenic amine contents generally increased in all treatments with increasing storage period. Significant differences were found (p < 0.01) in the levels of cadaverine, tyramine and histamine among the four treatments but it was not detected significant difference for putrescine, phenylethylamine and tryptamine in this level. Spermidine and spermine did not detect throughout the storage period for all experimental conditions. The amine contents of Atlantic bonito were highest in stored in cling film, followed by VP, MAP and chitosan film.

Effects of γ-irradiation upon biogenic amine formation in Egyptian ripened sausages during storage

The effects of γ-irradiation upon the biogenic amine inventory in Egyptian fermented sausages were investigated during storage for up to 30 days. Typical contents of biogenic amines in non-irradiated sausages ranged between 277 and 5815 mg/kgDW; irradiation with 2, 4 and 6 kGy decreased the total contents to 186–111, 188–98 and 180–57 mg/kgDW by the end of storage, respectively. Cadaverine was the major amine in non-irradiated samples — where it accounted for 44% of the total by 30 days; however, tyramine dominated in irradiated samples, where it accounted for 50%. On the other hand, the histamine content in non-irradiated sausage by 30 days of storage (i.e. 768 mg/kgDW) clearly exceeded the maximum allowable of 100 mg/kg, unlike happened in their irradiated counterparts. Therefore, the dramatic reduction observed in the histamine levels suggests that the use of this preservation technique will be beneficial for such a traditional processed meat. Industrial relevance: Traditional fermented sausages are a major food product in the Egyptian market, which consists of more that 70 million people. However, there are safety problems regarding this product owing to microbial contamination during processing that leads to biogenic amines; fermentation resorts only to its adventitious microflora (which in addition effect proteolysis, thus releasing free amino acids) and no thermal treatments are allowed (that would disturb its unique flavour). Hence, irradiation is in principle a promising alternative for industrial level production — viz. in controlling said biogenic amines. This manuscript addresses the lack of data in this particular field of obvious industrial interest.

Control of biogenic amines in food--existing and emerging approaches.

Biogenic amines have been reported in a variety of foods, such as fish, meat, cheese, vegetables, and wines. They are described as low molecular weight organic bases with aliphatic, aromatic, and heterocyclic structures. The most common biogenic amines found in foods are histamine, tyramine, cadaverine, 2-phenylethylamine, spermine, spermidine, putrescine, tryptamine, and agmatine. In addition octopamine and dopamine have been found in meat and meat products and fish. The formation of biogenic amines in food by the microbial decarboxylation of amino acids can result in consumers suffering allergic reactions, characterized by difficulty in breathing, itching, rash, vomiting, fever, and hypertension. Traditionally, biogenic amine formation in food has been prevented, primarily by limiting microbial growth through chilling and freezing. However, for many fishing based subsistence populations, such measures are not practical. Therefore, secondary control measures to prevent biogenic amine formation in foods or to reduce their levels once formed need to be considered as alternatives. Such approaches to limit microbial growth may include hydrostatic pressures, irradiation, controlled atmosphere packaging, or the use of food additives. Histamine may potentially be degraded by the use of bacterial amine oxidase or amine-negative bacteria. Only some will be cost-effective and practical for use in subsistence populations.

Biogenic amine formation in Turkish dry fermented sausage (sucuk) as affected by nisin and nitrite

The effects of nitrite (0, 100, and 200 mg kg(-1)) and nisin (0, 250, and 500 mg kg(-1)) on biogenic amine formation in sucuk were investigated by utilising a central composite design of response surface methodology. The addition of nitrite led to decreased levels of tryptamine, 2-phenylethylamine, putrescine, cadaverine, tyramine, and histamine, whereas nisin decreased the tryptamine level and counts of lactic acid bacteria. However, nisin increased putrescine, cadaverine, and spermidine levels. Their interactive effect was also found to be significant (P < 0.05) for putrescine values. The additional nitrite levels can be decreased by the addition of nisin, which will hinder biogenic amine formation.

Dimethylamine, Trimethylamine, and Biogenic Amine Formation in High‐Pressure Processed Semidried Squid (Todarodes pacificius) during Refrigerated Storage

The quality properties of semidried squid treated with high-pressure processing (HPP) were investigated during refrigerated storage. The vacuum-packed semidried squid samples were subjected to 500 MPa for 0 min (HPP-0), 5 min (HPP-5), and 10 min (HPP-10) by using a custom-made high-pressure processor and stored at a refrigerated temperature for 28 d. The populations of indigenous psychrotrophic and mesophilic bacteria were effectively reduced by approximately 1 and 2 log CFU/g at the HPP-10 treatment, respectively. Compared to the control, the bacterial counts in HPP-treated semidried squid samples were maintained at low levels throughout the storage period. The increase in the amounts of dimethylamine (DMA) and trimethylamine (TMA) was more pronounced at the unpressurized control than at the HPP treatments. The production of biogenic amines (BAs) varied with HPP treatment during refrigerated storage. Therefore, the application of HPP may provide a significant improvement in the safety and quality of semidried squid.

Characterization of Biogenic Amines and Factors Influencing Their Formation in Traditional Chinese Sausages

Biogenic amines in 42 traditional Chinese sausage samples obtained from different regions were determined by HPLC. The result showed that cadaverine was the major amine, followed by tyramine and putrescine. A total of 4 groups of samples were identified on the basis of total amines by cluster analysis. Group A included samples showing low amine contents (76.5 to 220 mg/kg) and accounted for 28.5% of the sausages examined. Group B included samples with moderate amine contents (220 to 600 mg/kg) and accounted for 45.2%. Group C included 11.9% of the samples showing high total biogenic amines contents (600 to 1000 mg/kg) and group D contained 14.28% of the samples showing very high levels of biogenic amines (higher than 1000 mg/kg). High correlation coefficients were found between the total counts of Enterobacteria and concentrations of total biogenic amines (r = 0.73). Sanitary quality of raw materials and the specific flora are import factors influencing biogenic amines formation in traditional Chinese sausages. Practical Application: Biogenic amines are considered potentially harmful substances to human health worldwide and are usually found in fermented sausage.Traditional Chinese sausage is one form of spontaneously fermented sausage and manufactured in small-scale plants following spontaneous fermentation. Little information, however, exists on the traditional Chinese sausage.

Influence of oenological practices on the formation of biogenic amines in quality red wines

Changes in the contents of biogenic amines (histamine, putrescine, tyramine, cadaverine, agmatine, ethylamine, isobutylamine, phenyletilamine, isoamylamine, serotonine and tryptamine) were studied during the winemaking process of quality red wines, including an organic wine. The analytical method used was validated in terms of linearity, precision, coefficient of variation and recovery. The limits of detection and quantification of the amines were also calculated. The method involved pre-column automated derivatisation of the amines by treatment with o-phthalaldehyde, after which the derivatives formed were analysed by reverse-phase HPLC. Results showed that grape must already contains biogenic amines and this content tends to increase throughout winemaking and maturation. The organic wine showed higher levels of biogenic amines than the non-organic wine. The fact that malolactic fermentation occurs spontaneously in organic wines, together with low levels of SO 2 because of legal restrictions, could be responsible for the higher levels in biogenic amines found. For the non-organic wine, 2 oenological practices could increase the content in biogenic amines: the addition of press wine to the free run wine, and the treatment with yeast mannoproteins.

Effect of fermentation with mixed starter cultures on biogenic amines in bighead carp surimi

SummaryThe effects of one group mixed starter cultures, combined with Lactobacillus casei, Streptococcus lactis, Saccharomyces cerevisiae Hansen, and Monascus anka, and a batch without starter as control on biogenic amines accumulation in the bighead carp surimi during fermentation were investigated. Determination of five different biogenic amines was carried out by reverse‐phase high‐performance liquid chromatography with UV detection. Results showed that mixed starter cultures decreased the pH quickly from initial pH value of 6.4 to 5.2, inhibited the growth of contaminant microorganisms, such as Enterobacteriaceae and Pseudomonas, present in the raw materials, and suppressed the accumulation of histamine, tyramines, spermine and spermidine. Fermentation inoculated with combination of Lactobacillus casei, Streptococcus lactis, Saccharomyces cerevisiae Hansen, and Monascus anka with negative‐decarboxylase activity may prevent biogenic amine formation in the fermented ssurimi and improve hygienic quality of fermented surimi.

Technological conditions influence aminogenesis during spontaneous sausage fermentation

The influence of two manufacturing processes on biogenic amine formation during the manufacture of Spanish dry fermented sausages of different diameters (fuet and llonganissa) was evaluated to elucidate which conditions allow better control of the aminogenic activity of spontaneous microbiota. Technological conditions affected both the amounts and the qualitative profile of biogenic amine accumulated. The higher processing temperature and relative humidity in process A (simulating those applied in industrial manufacture) favoured aminogenesis, since biogenic amine accumulation was faster and higher than in sausages manufactured under the process B (close to those used in traditional practices). The major amine differed depending on the diameter of the sausages, tyramine being the major amine in fuet (2.5 cm diameter sausage), and putrescine in llonganissa (4.5 cm). Moreover, sausages of higher diameter (llonganissa) had higher biogenic amine contents compared with the thinnest sausages (fuet). Conditions would modulate biogenic amine accumulation not only due to its influence on development of the bacterial population but also on its aminogenic activity. From the biogenic amine point of view, when sausages are spontaneously fermented, traditional lower temperatures and relative humidities are more appropriate than those usually applied in industrial processes.

The effect of different starter cultures and ripening temperatures on formation of biogenic amine in Turkish fermented sausages

Different starter culture added groups (Group I: Lactobacillus sake, Staphylococcus xylosus; Group II: Lactobacillus plantarum, Staphylococcus carnosus; Group III: Lactobacillus curvatus, Staphylococcus carnosus, and Staphylococcus xylosus) and control group sausage samples were produced experimentally at two different temperatures (22 and 26 °C). In raw materials and all groups, by the 0th, 2nd, 5th and 7th days of the ripening period, the analysis of HPLC and biogenic amine (tyramine, histamine, cadaverine, putrescine, phenylethylamine, tryptamine, spermine, and spermidine) amounts, microbiological (Lactic acid bacteria, Micrococcus/Staphylococcus, Enterobacteriaceae, Enterococcus spp., and moulds–yeasts) and chemical (pH, dry matter, and salt) have been done. During the ripening period, there is no statistical discrepancy (P > 0.05) in terms of biogenic amine amounts, microbiological, and chemical values detected from the sausage samples produced at 26 and 22 °C. However, in both levels of temperature, there is statistical discrepancy (P 0.05) for all values but the use of starter culture prevents the formation of biogenic amine in Turkish fermented sausages.

Formation of Biogenic Amines in Chicken Meat Stored under Modified Atmosphere

The aim of the study was to investigate the effects of two modified atmospheres with a different combination of gases on selected groups of microorganisms and on concentrations of biogenic amines (BAs) in samples of poultry breast muscle. The samples were packaged under modified atmosphere A (75% O2 a 25% CO2) or B (75% N2 and 25% CO2) and stored at temperatures from +2 to +4 °C for 14 days. During the storage period, O2 concentrations in modified atmosphere A (MA A) decreased from the initial 74.8 ± 0.3% to 55.9 ± 6.6% at the end of the storage period. In all samples, counts of psychrotrophic bacteria counts, Brochothrix thermosphacta, lactic acid bacteria and coliform microorganism were determined. The tests were made on the packaging day, and then after three, nine and fourteen days of storage. At the end of the storage period, higher numbers of psychrotrophic bacteria (6.5 ± 0.7 log10 cfu g-1), Brochothrix thermosphacta (4.8 ± 0.3 log10 cfu g-1) and lactic acid bacteria (1.7 ± 0.4 log10 cfu g-1) were found on samples packaged under MA A. Samples packaged under modified atmosphere B on the other hand contained higher numbers of coliform bacteria (4.1 ± 0.6 log10 cfu g-1) at the end of the storage period. In addition to microbiological indicators, concentrations of biogenic amines (putrescine, cadaverine, histamine, tyramine, spermine, spermidine and β-phenylethylamine) were also determined. In fresh samples and after three days of storage, only spermine and spermidine were found. After 9 and 14 days, also other BAs were detected. The biogenic amine totals at the end of the storage period was 60.0 ± 13.2 mg kg-1 in samples packaged under MA A and 129.0 ± 41.3 mg kg-1 in samples packaged under MA B. The most abundantly represented biogenic amines in samples packaged under MA A were putrescine and spermine (49.7 and 24.8%, respectively, at the end of the storage period), and putrescine and cadaverine in samples packaged under MA B (47.0 and 32.9 %, respectively, at the end of the storage period).

Biogenic Amine Production in Olomouc Curd Cheese (Olomoucké tvarůžky) at Various Storage Conditions

The aim of this study was to evaluate the effects of temperature and storage time on the formation of biogenic amines (BAs) in the traditional Czech curd cheese (Olomoucké tvarůžky). Samples were stored for 7 weeks at 5 °C and 20 °C. BAs were studied as dansyl derivatives by the RP-HPLC method with fluorescence detection, histamine was determined using a photodiode array detector. Physical and chemical properties were analyzed as specified by the Czech National Standard, as were the sensory characteristics (colour, odour, texture and flavour). The major amines found were cadaverine (124–2413 mg kg-1) and tyramine (117–1058 mg kg-1), followed by putrescine (75–767 mg kg-1) and histamine (74–411 mg kg-1). Low concentrations of tryptamine, spermine and spermidine were present. Total concentrations of BAs significantly increased with storage time (P &lt; 0.01), depending significantly on temperature (P &lt; 0.01). Total BAs in cheese stored at 20 °C compared to 5 °C were more than three times higher, reaching 4600 mg kg-1 at the end of storage. The toxicologically critical value of 900 mg kg-1 for the sum of histamine + tyramine + putrescine + cadaverine was reached 17 days later in the cheese stored at 5 °C compared to 20 °C. When stored at 5 °C, the samples retained adequate sensory characteristics for the entire safe storage time. The effects of storage conditions on BAs formation are relevant to reducing the risk associated with consumption of cheese high in BAs.

Formation of biogenic amines by Gram-negative bacteria isolated from poultry skin

The aim of this study is to explore production of biogenic amines (histamine, tyramine, putrescine, cadaverine, agmatine, spermine and spermidine) by 88 Gram-negative bacteria isolated from poultry skin (41 isolates of family Enterobacteriaceae, 21 isolates of genus Aeromonas, 16 isolates of genus Pseudomonas, and 10 isolates of other Gram-negative rods). Ion-exchange chromatography was employed to analyse the above mentioned amines. Enterobacteria were found to be the largest producers of amines with proved presence of tyramine, agmatine, putrescine, and cadaverine in cultivation broth after incubation of bacteria. Putrescine and cadaverine were the most abundant products. Presence of at least two biogenic amines, i.e. mainly concurrent presence of putrescine and cadaverine, was revealed in 19 enterobacteria strains. Eleven isolates classified into Aeromonas genus produced putrescine and five of them also formed cadaverine. The other observed biogenic amines (histamine, spermine and spermidine) were not found among tested isolates. Production of biogenic amines by any Pseudomonas family isolates was not proved.

The effects of ice storage on inosine monophosphate, inosine, hypoxanthine, and biogenic amine formation in European catfish (Silurus glanis) fillets

SummaryEuropean catfish fillets in ice were evaluated by measuring nucleotide components and biogenic amine contents and these then compared with sensory and microbiological assessment during the 21 days of iced storage. Analyses were carried out using two different rapid HPLC methods for nucleotid degradation products and biogenic amine contents in European catfish fillets. Sensory evaluation showed that storage life of European catfish found to be 14–18 days. Initial inosine monophosphate (IMP) level was 12.6 μmol g­1 and then decreased during the rest of storage period. Inosine (INO) level increased rapidly until 7 days of storage. Hypoxanthine (Hx) level increased almost linearly with storage time. The most accumulated biogenic amines were putrescine, cadaverine, spermidine, spermine, and serotonin in all the European catfish fillets during the storage, although the formation of biogenic amines levels was fluctuated. Histamine was only detectable at 4 and 7 days of storage as low as 1 mg 100 g­1 fish. Total viable count in European catfish increased rapidly with storage time and reached ≤109 cfu g­1 when the fillets were not acceptable for consumption.