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.
Similar content being viewed by others
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.
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
References
Akpomie OO, Okonkwo KE, Gbemre AC, Akpomie KG, Ghosh S, Ahmadi S, Banach AM (2021) Thermotolerance and cellulolytic activity of fungi isolated from soils/waste materials in the industrial region of Nigeria. Curr Microbiol 78:2660–2671. https://doi.org/10.1007/s00284-021-02528-3
Benkerroum N (2016) Biogenic amines in dairy products: origin, incidence, and control means. Compr Rev Food Sci Food Saf 15(4):801–826. https://doi.org/10.1111/1541-4337.12212
Curiel JA, Ruiz-Capillas C, de las Rivas B, Carrascosa AV, Jimenez-Colmenero F, Munoz R (2011) Production of biogenic amines by lactic acid bacteria and Enterobacteria isolated from fresh pork sausages packaged in different atmospheres and kept under refrigeration. Meat Sci 88(3):368–373. https://doi.org/10.1016/j.meatsci.2011.01.011
Erdag D, Merhan O, Yildiz B (2019) Biochemical and pharmacological properties of biogenic amines. In: Proestos C (ed) Biogenic amines. Intech Open, Athens, Greece
Espinosa-Pesqueira D, Roig-Sagues AX, Hernandez-Herrero MM (2018) Screening method to evaluate amino acid-decarboxylase activity of bacteria present in Spanish artisanal ripened cheeses. Foods. https://doi.org/10.3390/foods7110182
FAO (2015) The state of food insecurity in the world 2015. Meeting the 2015 International Hunger targets: taking stock of uneven progress. Food and Agricultural Organisation, Rome
Fernandez-Reina A, Urdiales JL, Sanchez-Jimenez F (2018) What we know and what we need to know about aromatic and cationic biogenic amines in the gastrointestinal tract. Foods. https://doi.org/10.3390/foods7090145
Ghosh S, Kam G, Nijjer M, Stenner C, Cheeptham N (2020) Culture dependent analysis of bacterial diversity in Canada’s raspberry rising cave revealed antimicrobial properties. Int J Speleol 49(1):43–53. https://doi.org/10.5038/1827-806X.49.1.2291
Ghosh S, Paine E, Wall R, Kam G, Lauriente T, Sa-ngarmangkang PC, Horne D, Cheeptham N (2017) In situ cultured bacterial diversity from iron Curtain Cave, Chilliwack, British Columbia. Can Divers 9(36):1–15. https://doi.org/10.3390/d9030036
Gonzalez-Jimenez M, Arenas-Valganon J, Garcia-Santos Mdel P, Calle E, Casado J (2017) Mutagenic products are promoted in the nitrosation of tyramine. Food Chem 216:60–65. https://doi.org/10.1016/j.foodchem.2016.08.006
HPLE (2014) Food losses and waste in context of sustainable food systems: high level panel experts on food security and nutrition of the committee on World Food Security, Rome, Italy
Huang YR, Liu K-J, Hsieh H-S, Hsieh C-H, Hwang D-F, Tasi Y-H (2010) Histamine level and histamine-forming bacteria in dried fish products sold in Penghu Island of Taiwan. Food Contol 21:1234–1239. https://doi.org/10.1016/j.foodcont.2010.02.008
Kuiper M, Cui HD (2020) Using food loss reduction to reach food security and environmental objectives—a search for processing leverage points. Food Policy 98:101915. https://doi.org/10.1016/j.foodpol.2020.101915
Li L, Wen X, Wen Z, Chen S, Wang L, Wei X (2018) Evaluation of the Biogenic amines formation and degradation abilities of Lactobacillus curvatus From Chinese Bacon. Front Microbiol 9:1015. https://doi.org/10.3389/fmicb.2018.01015
Linares DM, Del Rio B, Ladero V, Martinez N, Fernandez M, Martin MC, Alvarez MA (2012) Factors influencing biogenic amines accumulation in dairy products. Front Microbiol 3:180. doi:https://doi.org/10.3389/fmicb.2012.00180
Mohammed GI, Bashammakh AS, Alsibaai AA, Alwael H, El-Shahawi MS (2016) A critical overview on the chemistry, clean-up and recent advances in analysis of biogenic amines in foodstuffs. TRAC Trends Anal Chem 78:84–94. https://doi.org/10.1016/j.trac.2016.02.007
Ojeh VN, Ojoh CO (2011) Impact of climate variability on road transport in Warri Metropolis. Int J Environ Sci 2(27):988–995
Özogula Y, Özogul F (2019) Biogenic amines formation, toxicity, regulations in food. Biogenic amines in food: analysis, occurrence and toxicity. Food Chemistry, Function and Analysis. The Royal Society of Chemistry, pp 1–17. https://doi.org/10.1039/9781788015813-00001
Pessione E, Cirrincione S (2016) Bioactive molecules released in food by lactic acid bacteria: encrypted peptides and biogenic amines. Front Microbiol 7:876. https://doi.org/10.3389/fmicb.2016.00876
Raak N, Symmank C, Zalu S, Aschemann-Witzel J, Rohm H (2017) Processing and product related causes for the food supply chain. Waste Manag 61:461–472. https://doi.org/10.1016/j.wasman.2016.12.027
Ruiz-Capillas C, Herrero AM (2019) Impact of biogenic amines on food quality and safety. Foods 8(2):62. https://doi.org/10.3390/foods8020062
Russo P, Spano G, Arena MP, Capozzi V, Griew F, Abdbenduu L (2010) Are consumers aware of the risks related to biogenic amines on food? Microbiol Biotechnol 2:1087–1095
Schanes SK, Dobernig K, Goezet B (2018) Food waste matters—a systemic review of household food waste practices and their policy implication. J Clean Prod 182:978–991. https://doi.org/10.1016/j.jclepro.2018.02.030
Spang ES, Moreno LC, Pace SA, Achmin Y, Doris-Gonazalez I, Gosliner WA, Jablonski-Shefield MP, Monin MA, Quested TE, Winans KS, Tomich TP (2019) Food loss and waste: measurement, drivers and solutions. Annual Rev Environ Resour 44:117–156. https://doi.org/10.1146/annurev-environ-101718-033228
Standards NCfCL(2003) Approved Standard: M2-A8. Performance Standards for Antimicrobial Disk Susceptibility Tests. 8th Edition. National Committee for Clinical Laboratory Standards, Wayne
Suzzi G, Torriani S (2015) Editorial: Biogenic amines in foods. Front Microbiol 6:472. https://doi.org/10.3389/fmicb.2015.00472
Triki M, Herrero AM, Jimenez-Colmenero F, Ruiz-Capillas C (2018) Quality assessment of fresh meat from several species based on free amino acid and biogenic amine contents during chilled storage. Foods. https://doi.org/10.3390/foods7090132
Visciano P, Schirone M, Tofalo R, Suzzi G (2014) Histamine poisoning and control measures in fish and fishery products. Front Microbiol 5:500. https://doi.org/10.3389/fmicb.2014.00500
Yang Q, Meng J, Zhang W, Lui L, He L, Deng L, Zeng X, Ye C (2020) Effects of amino acid decarboxylase genes and pH on the amine formation of enteric bacteria from Chinese traditional fermented fish. Front Microbiol 11:1130. https://doi.org/10.3389/fmicb.2020.01130
Wójciak MK, Sokska E (2016) Evolution of free amino acids, biogenic amines and N-Nitrosamines throughout ageing in organic fermented beef. Acta Sci Pol Technol Aliment 15(2):191–200. https://doi.org/10.17306/J.AFS.2016.2.19
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.
Funding
No funding.
Author information
Authors and Affiliations
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.
Corresponding author
Ethics 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.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Akpomie, O.O., Ejechi, B.O., Banach, A.M. et al. Biogenic amine production from processed animal and plant protein-based foods contaminated with Escherichia coli and Enterococcus feacalis. J Food Sci Technol 59, 4880–4888 (2022). https://doi.org/10.1007/s13197-022-05576-0
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-022-05576-0