Abstract
The aim of the study was to investigate biogenic amine production in different types of cooked protein foods. The food samples were incubated at varying temperatures (4, 37 and 55 °C) on different microbiological media for 48, 72 and 180 h. Resulting bacteria were isolated and characterized using cultural, biochemical and molecular methods, further screened for production of biogenic amines in decarboxylase broth media supplemented with 0.4% of histidine, tyrosine, lysine and ornithine. The samples were incubated at 25 °C for 48 h and the biogenic amine concentration in each food sample determined by means of HPLC. There was a high prevalence of the isolates among the food samples. All the isolates except Klebsiella sp. and Pseudomonas sp. were positive for decarboxylase activity indicating 84.6% of the isolates capable of biogenic amine production. The amine concentration varied among the types of food and methods of cooking. Histamine was detected in 41.67% of the inoculated food samples (9.2 ± 1.2–100.95 ± 0.1 µg/g) while putrescine was the least detected (41.67%) in the inoculated food sample (7.7 ± 0.1–8.8 ± 0.2 µg/g). Cadaverine and histamine were detected in 16.4% (2.6 ± 0.2–49.9 ± 0.9 µg/g) and 7.5% (1.4 ± 0.1–20.4 ± 0.3 µg/g) of the foods, respectively. Microbial contamination of the cooked protein foods led to high levels of biogenic amines irrespective of the cooking methodology adopted and type of foods investigated.
Supplementary Information
The online version contains supplementary material available at 10.1007/s13197-022-05576-0.
Keywords: Biogenic amines, Cooked protein foods, Escherchia coli, Enterococcus feacalis
Introduction
The Federal Department of Agriculture (FDA) and the European Food Safety Authority (EFSA) target histamine (a biogenic amine) as one of the toxins (Triki et al. 2018). According to the WHO, more than 200 diseases are transmitted through food and significant part of the population is exposed to food borne diseases during their lifetime.
Biogenic Amines (BAs) are low molecular weight organic nitrogen compounds formed by decarboxylation of amino acids or by amination and transamination of aldehydes and ketones during normal metabolic processes in living cells. The following BAs are produced from the following amino acids: histamine from histidine, tyramine from tyrosine, tryptamine from serotonin, phenylethylamine from phenylalanine, putrescine from ornithine, cadaverine from lysine and agmatine from arginine (Pessione and Cirrincione 2016). BAs play important roles in assessing the quality and or acceptability of some foods, and the proper management of these qualities will guarantee and ensure food safety (Triki et al. 2018). They serve as nitrogen source and precursors for the synthesis of alkaloids, nucleic acids, proteins, amino acids, and food aroma components. However, when present in high concentrations, they might have toxicological effects, that include desire for chocolate, and health hazards which trigger vasoactive, psychoactive, respiratory disorders, headaches, tachycardia, hypo or hypertension, allergic reactions, headaches, tachycardia (Li et al. 2018). These toxicological and physiological effects of BAs make them a potential public health concern (Ruiz-Capillas and Herrero 2019).
BAs are found in all foods containing proteins or free amino acids such as fish and fish products, seafoods, meat and meat products—dry fermented meat, fresh meat, sausage, pork sausages, cheese, dairy nuts, dairy products, wine, beer, vegetables, soybeans and chocolate in varying concentrations (Triki et al. 2018). For instance, in a previous study it has been demonstrated that the histamine poisoning is one of the common forms of intoxication in canned, cooked fish and fish products because of its thermostable properties (Visciano et al. 2014). Additionally, the toxic effects of histamine are enhanced by other biogenic amines such as putrescine and cadaverine (Huang et al. 2010).
On the other hand, in accordance to WHO and CODEX standards the maximum amount of histamine that is allowed in fish and fish products according to the hygiene and handling indicator level is 200 mg/kg. However, different countries vary in their regulatory limits of biogenic amine levels in foods as a quality indicator and food safety. Therefore, BAs play vital roles in assessing the quality and/or acceptability of some foods, and management of these qualities will guarantee and ensure food safety (Triki et al. 2018).
Most of the organisms including plants, animals, microorganisms, and humans are capable of producing biogenic amines during normal metabolic processes. As they are considered to be the first step of protein, hormone, and nucleic acid biosynthesis, therefore the are the unique components of living cells and are required for the maintenance of the intestinal immunologic systems and healthy functioning of the metabolic processes (Erdag et al. 2019). Studies have shown that there are several factors that govern the production of biogenic amines in the foods (Linares et al. 2012). These include the presence of specific bacterial strains possessing specific activated catabolic pathways, environmental conditions that favor decarboxylase activities, availability of amino acid substrates, storage conditions, raw materials, manufacturing processes and temperature (Triki et al. 2018).
BAs formation in food is associated with food spoilage, resulting from poor hygienic practices, which could be an indication of implementing improper food safety measures (Benkerroum 2016). Studies exhibited that there are diverse groups of microorganisms isolated from foods associated with the production of biogenic amines. For instance, a study of Fernandez-Reina et al. (2018) has reported the production of histamine and tyramine by Lactobacillus casei in the skimmed milk samples. Ingestion of such food products containing the excess of BAs can lead to high levels of BAs in the organism (Fernandez-Reina et al. 2018).
The production of biogenic amines signifies food loss hence food insecurity. According to HPLE (2014), food loss and waste might lead to food insecurity (FAO 2015). The food loss through spoilage may be controlled by practices that will reduce food contact with microorganisms at different steps of processing. Kuiper and Cui (2020) reported leverage points for reduction in food loss and focused on domestic stages. Microbial food spoilage could eventually lead to food loss and food waste along the food supply chain (Spang et al. 2019). It can be prevented by targeting consumers’ and retailers’ behaviors (Raak et al. 2017).
A holistic solution approach was proposed by Schanes et al. (2018) to include setting of the policy measures for households, research, development, and medical sector to enhance food quality by averting the introduction of microorganisms including those capable of biogenic amine productions and ultimately resulting in food insecurity.
BAs can be used as good promoters of food spoilage. The presence of secondary amines, such as cadaverine and putrescine being good indices of food spoilage, can potentially lead to the toxicity of histamine, and the reaction with nitrites to form nitrosamine.
The study of biogenic amines in Nigeria is still at its prelude, especially in estimating the levels of BAs in the local foods, although previous studies made some preliminary investigations mainly on fermented foods and meat products. The control of biogenic amines will ensure higher quality products with fewer health implications. Therefore, it is a prerequisite to determine the level of biogenic amines in indigenous foods of Nigeria, apart from the fermented foods in which microorganisms are expected to be present. The present study emphasizes in determining the biogenic amines from different types of cooked protein food products from the Warri area of Nigeria.
Materials and methods
Materials
The culture media and the amino acid standards (L-ornithine, L-lysine, L-tyrosine and L-histidine) were procured from Life Save Biotech (San Diego, USA) and Sigma Chemicals (Madrid, Spain), respectively, whereas the HPLC grade acetonitrile and methanol were obtained from Merck Chemicals (Darmstadt, Germany). The glacial acetic acid and filter paper were acquired from Merck Chemicals (La Couna, Spain) and Whatmann (Maidstone, England), respectively.
The HPLC apparatus, comprised of two L1−100 pump, a 20 µL rheodyne (Cotati, CA), injection loop, C18 Column heater, LC-100 UV-detector and a 4290 integrator connected to a computer, at the Research laboratory of Pharmaceutics and Industrial Pharmacy, Delta State University, Abraka.
Sample collection area
Warri is a city in South Western Nigeria, West Africa (latitude 5°′30′ N; longitude 5°48′ E, area: 1520 sq. miles, population: 500,000) being the hub of the oil and gas industry in Niger Delta State area of Nigeria. As the industrial and commercial center with frequent activities it fascinates both local and international personnel for investment; hence there is a boom in the hospitality industry in the form of hotels and restaurants (Ojeh and Ojoh 2011).
Sample collection
Five hotels were randomly selected from the indicated area and 6 samples each of food type, namely: fried chicken, fish, meat, boiled beans and two types of beans paste (steamed and fried) were collected in sterile polythene bags (in total 180 samples). The pH and temperature of the food samples were determined at the collection point. The samples were transported in ice packs to the Microbiology Laboratory, Delta State University, Abraka for further analyses.
Bacterial species isolation and cultivation
One gram of each sample was aseptically weighed and macerated using laboratory mortar and pestle. Decimal dilutions (10− 1 – 10− 10) of the samples were made in sterile physiological saline (0.9%) solution and 0.1 mL of the 10− 3 and 10− 4 dilutions were poured platted on the Nutrient agar, MacConkey’s Agar, Mannitol salt agar, de Man, Rogosa and Sharpe (MRS) agar media (LifeSave, Biotech, San-Diego, USA). The inoculated media were incubated at 4, 37 and 55 °C for 48, 72 and 168 h, respectively. The observed colonies were enumerated as per previous studies and morphologically identified based on the Bergey’s manual of determinative bacteriology. Furthermore, each of the isolates was cultivated as pure culture and the most abundant colonies were identified with 16S rRNA gene sequencing using 27F (5′-AGAGTTTGATCMTGGCTCAG-3′) and 1492R (5′-TACGGYTACCTTGTTACGACTT-3′) primers as per previous studies (Akpomie et al. 2021; Ghosh et al. 2017, 2020). Furthermore, the cultivated pure cultures were inoculated into 3 mL peptone water followed by incubation at 37 °C for 24 h. Following the incubation, the cells were harvested and rinsed three times in physiological saline solution. McFarland standard was used as a reference to adjust the turbidity of the bacterial suspensions in accordance to the methodology adopted by National Committee for Clinical Laboratory Standards (2003). Additionally, the cells density was also measured at OD530 in UV-Spectrophotometer (Shimadu, Japan) to adjust the inoculum size to 106 CFU/mL.
Assessment of amino acid decarboxylase activities
The bacterial cultures with the specific inoculum size were inoculated in the Nutrient broth (LifeSave Biotech, San-Diego, USA) supplemented with 0.4% each of histidine, tyrosine and ornithine and incubated at 26 ± 2 °C for 48 h. Following the incubation, 1 mL of each of the cultivated culture was spread plated on the decarboxylase agar media. The decarboxylase activities were observed by the purple/grey-purple translucent zone formed around the colonies indicating the formation of histamine or tyramine in an alkaline environment. The negative decarboxylase activities were evaluated by retaining of the yellow coloration around the colony (Espinosa-Pesqueira et al. 2018).
Confirmation of amino acid decarboxylase activities by HPLC
HPLC standard preparations
Each of the amines (0.001 g) was dissolved in 0.1 mL of glacial acetic acid and 9.9 mL of methanol to attain a final concentration of 100 µg/mL of the working solution. The solution was filtered and twofold dilution was performed to the sixth concentration to plot calibration curve. Similar solution was prepared for each of the macerated food samples deliberately contaminated with 0.1 mL of 0.5% McFarland standard inoculum of each of E. coli and Enterococcus faecalis and incubated for 72 h. The solutions were devoid of glacial acetic acid to ensure that the bioamines are the products of the microbial fermentation process. Following the incubation, the solutions were subjected to HPLC analysis. Contents of amines were expressed in µg per g of food sample.
Assessment of biogenic amines
The decarboxylase activity of the strains was confirmed by the quantitative biogenic amine analysis produced in the broth using an automated HPLC system (Shimadzu, Kyoto, Japan) equipped with a LC-100 pump, a 20 µL Rheodyne (Cotati CA), Injection loop, (18 column heater, LC-100 µv-vis detector and 4290 integrator. The HPLC analysis was carried out at a constant temperature of 25ºC using a gradient acetonitrile and methanol as mobile phase A and B, respectively. The working solution for the analysis was prepared by dissolving 0.1 mL of each of the samples in 0.1 mL of gradient acetonitrile which was further diluted with 9.9 mL of methanol. Three hundred microliter of the working solution of each sample was injected into C18 column at a steady flow rate of 0.500 mL/mm with a wavelength of 232 mm.
Statistical analysis
An independent sample t-test was conducted to investigate the difference in amine producing capacity of E. coli and E. faecalis. Additionally, one-way ANOVA with LSD post hoc test was performed to assess the difference between the food samples’ concentration and methods of preparation. All analyses were conducted using IBM SPSS Version 23 (USA). Significance was assumed at p < 0.05, values were presented as means (n = 6) ± standard deviation (SD).
Results
Physical properties of studied food
The food samples were characterized by semi-neutral pH. The highest pH was recorded for fried fish, fried chicken and cooked beans. All the studied food samples had pH ranging from 6.6 ± 0.02–6.2 ± 1.00 with fried fish and meat bearing a pH of 6.6 ± 0.02 and 6.2 ± 0.02, respectively, while fried chicken was estimated a pH of 6.5 ± 0.20. The fired beans (Akara) and steamed beans paste (moi-moi) were noted with an identical pH of 6.2 ± 1.00 while cooked beans was estimated with 6.5 ± 1.00.
Identification of the microorganisms
The Gram’s characteristics identified cocci and rod shaped as Gram positive and negative bacteria, respectively. According to the Bergey’s manual of determinative bacteriology, the isolates were identified as Escherichia coli, E. faecalis, Salmonella sp., Klebsiella sp., Morganella sp., Enterobacter sp., Shigella sp., Listeria monocytogenes, Lactobacillus brevis, Campylobacter sp., Pseudomonas sp., Bacillus subtilis and Leuconostoc sp. (Table 1). Furthermore, 16 S rRNA gene sequencing of the most abundant colonies (Table 2) revealed close resemblance to the bacterial homologues E. coli (Identity: 84.44%; Query coverage: 100%) and E. faecalis (Identity: 99.66%; Query coverage: 96%).
Table 1.
Identification of the isolates from various food samples
| Morphology | Biochemical test | Probable identity of Isolates | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Gram reaction | Oxidase | Catalase | Indole | Motility | Citrate | Glucose | Lactose | H 2S | ACID | GAS | ||
| Rod | – | – | + | + | + | – | + | + | – | + | + | Escherichia coli |
| Cocci (short chain) | – | – | – | – | – | – | + | + | – | – | + | Enterococcus faecalis |
| Rod | – | – | + | + | + | + | – | – | + | + | – | Salmonella sp. |
| Rod | + | – | + | – | – | + | + | + | + | – | – | Klebsiella sp. |
| Rod | + | – | + | – | + | – | + | + | + | – | – | Morganella sp. |
| Rod | – | – | + | – | + | + | + | + | – | + | + | Enterobacter sp. |
| Rod | – | – | + | – | – | – | – | – | – | + | – | Shigella sp. |
| Rod (curved rods) | – | + | + | – | + | + | – | – | + | + | – | Campylobacter sp. |
| Rod (long chain) | + | – | – | + | – | – | – | + | + | – | – | Listeria monocytogenes |
| Rod | + | – | – | + | – | + | + | – | – | + | + | Lactobacillus brevis |
| Rod | – | + | + | – | + | + | + | + | – | + | – | Pseudomonas sp. |
| Rod | + | – | + | – | + | + | + | + | – | + | – | Bacillus subtilis |
| Cocci | + | – | – | – | – | – | + | + | – | + | + | Leuconostoc sp. |
‘+’ and ‘–’ denotes ‘presence’ and ‘absence’, respectively
Table 2.
Sources and prevalence of isolated bacteria
| Sample | Fried fish | Fried meat | Fried chicken | Beans | Steamed beans paste | Fried beans paste | Prevalence % |
|---|---|---|---|---|---|---|---|
| Escherichia coli | + | + | + | + | + | + | 100.0 |
| Enterococcus faecalis | + | + | + | + | + | + | 100.0 |
| Salmonella sp. | + | – | + | – | + | + | 66.7 |
| Klebsiella sp. | + | – | – | + | + | – | 50.0 |
| Morganella sp. | + | + | – | – | – | – | 33.3 |
| Enterobacter sp. | + | – | – | – | – | – | 6.7 |
| Shigella sp. | + | + | – | – | – | + | 50.0 |
| Campylobacter sp. | + | – | – | – | – | – | 16.7 |
| Listeria sp. | + | – | + | – | – | – | 33.3 |
| Lactobacillus sp. | + | + | – | + | – | – | 33.3 |
| Pseudomonas sp. | + | + | – | – | – | + | 33.3 |
| Bacillus sp. | + | – | – | – | + | + | 33.3 |
| Leuconostoc sp. | + | – | – | + | + | – | 33.3 |
‘+’ and ‘–‘ denotes ‘presence’ and ‘absence’ of the microorganisms, respectively
Distribution of bacteria on food
Escherichia coli and Enterococcus sp. populated maximally (100%) of all the food samples followed by Salmonella sp. (66.7%). Both Klebsiella sp. and Shigella sp. accounted for 50% of the population while rest of the microbes accounted only for 33.33% (Table 2). Notably, fried fish exhibited the maximum occurrence of bacteria while fried chicken harbor the least (four bacterial species). Beans displayed five bacterial species while the rest showed six types (Table 2).
Microbial growth and enzymatic activity
All microbes grew at 35–37 °C except Campylobacter sp. and Listeria sp. The temperature of 4–10 °C supported only the growth of Listeria sp. while Campylobacter sp. and Bacillus sp. colonized at 45–55 °C. All the bacteria were positive for decarboxylase activity except Klebsiella sp., Listeria sp., and Pseudomonas sp. (Table 3).
Table 3.
Screening for decarboxylase activity of isolates at different temperature ranges
| Isolates | Temperature (°C) ranges | Enzymatic activities | ||
|---|---|---|---|---|
| 4–10 | 35–37 | 45–55 | Decarboxylase | |
| E. coli | NG | G | NG | + |
| E. faecalis | NG | G | NG | + |
| Salmonella sp. | NG | G | NG | + |
| Klebsiella sp. | NG | G | NG | – |
| Morganella sp. | NG | G | NG | + |
| Enterobacter sp. | NG | G | NG | + |
| Shigella sp. | NG | G | NG | + |
| Campylobacter sp. | NG | NG | G | + |
| Listeria sp. | G | NG | NG | – |
| Lactobacillus sp. | NG | G | NG | + |
| Pseudomonas sp. | NG | G | NG | – |
| Bacillus sp. | NG | G | G | + |
| Leuconostoc sp. | NG | G | NG | + |
NG, G, + and – depicts ‘no growth’, ‘growth’ ‘present’ and ‘absent’, respectively
Determination of Biogenic Amines
The concentrations of biogenic amines detected in the inoculated food samples were higher in comparison to the non-inoculated ones (Tables 4, 5). There was a significant increase in the levels of histamine in the contaminated food samples (p < 0.01) while tyramine was not detected in any of the foods samples before and after the inoculation. We have found the highest levels of histamine in food samples contaminated with E. coli for boiled beans, fish and steamed beans paste being significantly (p < 0.01) higher than for those contaminated with E. faecalis. There was no significant difference in the levels of cadaverine before and after inoculation (p = 0.24) while putrescine was detected only in steamed beans paste and fried beans paste inoculated with E. faecalis (p < 0.001).
Table 4.
Concentration of amines in the non-inoculated food samples (µg/g)
| Food Sample | Histamine | Tyramine | Cadaverine | Putrescine |
|---|---|---|---|---|
| Fried fish | ND | ND | 3.0 ± 0.3 | ND |
| Fried meat | ND | ND | ND | ND |
| Fried chicken | ND | ND | ND | ND |
| Boiled beans | ND | ND | 3.1 ± 0.9 | ND |
| Steamed beans paste (Moimoi) | ND | ND | ND | ND |
| Fried beans paste (Akara) | 1.4 ± 0.1 | ND | ND | ND |
ND Not detected
Table 5.
Concentration of amines in foods contaminated with Enterococcus faecalis. and E. coli (µg/g)
| Food organism | Histidine (histamine) |
Tyrosine (tyramine) | Lysine (cadaverine) |
Ornithine (putrescine) |
|---|---|---|---|---|
| Fish + E. coli | 98.3 ± 0.2 | ND | 3.0 ± 0.1 | ND |
| Fried meat + E. coli | ND | ND | ND | ND |
| Fried chicken + E. coli | ND | ND | ND | ND |
| Boiled beans + E. coli | 100.9 ± 0.1 | ND | 2.9 ± 0.1 | ND |
| Steamed beans paste + E. coli | 36.5 + 0.1 | ND | 2.7 ± 0.2 | ND |
| Fried beans paste + E. coli | ND | ND | 3.6 ± 0.1 | ND |
| Fried fish + E. faecalis | ND | ND | 4.5 ± 0.2 | ND |
| Friend meat + E. faecalis | 9.2 ± 1.2 | ND | ND | ND |
| Fried chicken + E. faecalis | ND | ND | ND | ND |
| Steamed beans paste + E. faecalis | 19.7 ± 0.2 | ND | ND | 7.7 ± 0.1 |
| Boiled beans + E. faecalis | ND | ND | 2.9 ± 0.2 | ND |
| Fried beans paste + E. faecalis | ND | ND | 3.2 ± 0.2 | 8.8 ± 22 |
ND Not detected
Discussion
The present study exhibited isolation of a diverse range of microorganisms from the collected food samples. Among them Enterobacter sp., E. faecalis, Escherichia sp., Shigella sp., Staphylococcus sp. and Klebsiella sp. were more prevalent in comparison to others. The growth of the microorganisms might have been supported by the favorable growth conditions present in the food such as the organic nutrient content (mainly protein in this study), pH, temperature and moisture content. Triki et al. (2018) reported that optimum pH, temperature of 20–37 °C, time and prolonged storage make food more susceptible to amine formation. Yang et al. (2020) reported that the optimum pH for decarboxylase activity is 5.0–6.5. Most of these organisms were positive for decarboxylase activity indicating their ability to produce biogenic amines. This might have been enhanced by conditions such as a neutral pH of 6.2–6.6, a temperature of about 28 ± 2 °C, presence of amino acids present in the protein foods present in the food which enabled the production of the enzyme for the amino acid decarboxylation and subsequent biogenic amines production. A previous study (Benkerroum 2016) has outlined the factors that influenced the BAs production which include the presence of bacterial strains, level of decarboxylation activities occurred, availability of amino acid substrates, storage, and environmental conditions favorable to decarboxylation activity (Linares et al. 2012). These factors also explained why some microbes exhibited negative decarboxylase activities in the current study. Ability to produce biogenic amines could also be correlated to the presence of corresponding amino acid/decarboxylase genes. For instance, in earlier study (Curiel et al. 2011) researchers have isolated bacteria belonging to Enterobacteriaceae and Lactic acid bacteria (LAB) species capable of producing putrescine and cadaverine. The synthesis of these compounds could be associated to the presence of the decarboxylase gene depending on the substrate. Yang et al. (2020) studied the effects of amino acid decarboxylase genes on amine production. They reported that amine production is dependent on the available decarboxylase genes such as odc, speA, spB, adiA, hdc and hisRC genes.
The presence of identified microorganisms especially E. faecalis and E. coli was predominant and may be traced to low hygienic manufacturing practices and poor storage conditions such as improper handling of foods, contaminated equipment and surfaces on which the food was prepared. Earlier study (Yang et al. 2020) hase exhibited the production of putrescine in food associated with the presence of specifically Pseudomonas sp. and Enterobacteriaceae. Unlikely, in our study Pseudomonas sp. did not produce any biogenic amines what could be attributed to the strain specificity and the source of the free amino acids. Conversely, the ability of E. coli and E. faecalis isolated in the present study to produce BAs could be assigned to their possible qualities for possessing decarboxylase activity. It is a positive factor influencing BAs production supported by the earlier study that showed the presence of decarboxylate positive microorganisms in food was (Linares et al. 2012).
On the other hand it has also been determined that the concentration of the precursor amino acids indicate the presence of amines in the food (Suzzi and Torriani 2015). Some bacteria such as LAB can hydrolyze proteins to release free amino acids and their carboxylases can further catalyze amino acids to BAs. Some LAB can synthesize amine oxidases to degrade biogenic amines. The increase the levels of biogenic amines in the food after the microbial introduction might be an indication of the their ability to decarboxylate the free substrate amino acids using appropriate metabolic pathways in a favorable environment (Russo et al. 2010). Different strains of bacteria possess different capabilities to form biogenic amines and for the degradation. BAs are regarded as food hazards (Özogula and Özogul 2019). Spermine, spermidine, tyramine, 2-phenylalanine, histamine, putrescine, tryptamine, cadaverine have been reported as the most important BAs in foods and mainly produced by microbial decarboxylation of amino acids (Mohammed et al. 2016).
The production of relatively high levels of the BAs (histamine, cadaverine and ornithine) has been reported. These have indicated deterioration of food products, accumulation of toxic metabolites, resulting in food insecurity. The danger associated with contamination of foods with microorganisms capable of decarboxylation is that over time there might be an increase in the level of amine production which may eventually lead to a higher level than initially detected in the food. At 100–800 mg/kg of tyramine and histamine in the food, their consumption may be hazardous to health and even fatal. Cadaverine causes headaches, respiratory disorders and allergic reactions, presence of tyramine can lead to high blood pressure and vasoconstriction. Other health hazards of BAs include triggering psychoactive, vasoactive and hypertension effects (Gonzalez-Jimenez et al. 2017). The production of biogenic amines in foods which could have been triggered by microbial contamination can cause food spoilage hence food insecurity. Some toxicological effects and outbreaks of foodborne illnesses have been linked histamine and tyramine. Secondary amines in food may form nitrosamines via nitrosation. Nitrosamines react with Deoxyribonucleic acid and have been found to be carcinogenic (Wojciak and Sokska 2016).
Conclusion
The food samples used in this study contained biogenic amines but at low levels. However, when contaminated with E. coli and E. faecalis which were the predominant isolates, there was a substantial increase in the concentration of histamine. Most of the organisms isolated were capable of decarboxylation activity but at varying degrees, which suggests the ability to produce biogenic amines when food is contaminated with them. The growth of all the isolates except Listeria sp. was inhibited at the low temperature suggesting that the storage at low temperature (e.g. in the refrigerator) will inhibit the growth of the organisms hence production of biogenic amines. Symptoms of biogenic amine consumption especially histamine are similar to those of other diseases, hence can be wrongly diagnosed. The wrong diagnoses can be due to lack of inadequate facilities, expertise and fund which are some of the challenges faced by the health sectors in developing countries. In order to safeguard the populace against public health risk associated with the consumption of suspected foods, there is a need to ensure good personal hygienic and manufacturing practices at all stages of production, retailing and storage.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
We are thankful to Dr. Swagata Ghosh, Assistant Professor of English, Symbiosis Institute of Technology, Symbiosis International University, Pune, India for editing this manuscript.
Abbreviations
- ANOVA
Analysis of variance
- CODEX
Codex alimentarius commission
- BAs
Biogenic amines
- EFSA
European Food Safety Authority
- FDA
Federal Department of Agriculture
- FAO
Food and Agriculture Organisation of the United Nations
- HPLE
Health Professionals Competency Assessment & Licensure Directorate
- HPLC
High Performance Liquid Chromatography
- LSD
Least Significant Difference
- MRS
de Man, Rogosa and Sharpe
- WHO
World Health Organisation
Authors’ contributions
OOA and SG conceived the study and designed the experiments. IA, OOA and BOE conducted all the experiments. SG drafted the manuscript. SG, AMB, EDA, OOA, SA and KGA read and edited the manuscript.
Funding
No funding.
Data availability
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
Declarations
Conflict of interest
The authors declare no financial interest nor conflict of interest.
Ethical approval
Not applicable.
Consent to participate
All the authors have given consent to participate.
Consent for publication
All authors approve to submit and publication to the journal.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
Not applicable.