Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 1

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

Molecular Identification and Biogenic Amine Production Capacity of Enterococcus faecalis Strains Isolated from Raw Milk

Wiśniewski, Patryk, Barbieri, Federica·2025·International Journal of Molecular Sciences
DOI 10.3390/ijms262110480
Open this paper in CoChat — free account

Abstract

In this study, Enterococcus faecalis strains isolated from raw cow’s milk were examined for genetic diversity, ability to produce biogenic amines (including histamine, tyramine, putrescine, cadaverine, 2-phenylethylamine) and the presence of corresponding amino acid decarboxylase genes. Identification of 29 strains obtained from Polish farms was carried out by polymerase chain reaction (PCR) and matrix-assisted laser desorption and ionization time of flight (MALDI-TOF MS) methods, and their genetic relationships were assessed by the Enterobacterial Repetitive Intergenic Consensus Polymerase Chain Reaction (ERIC-PCR) technique. Amine production capacity was assessed in vitro on synthetic medium, while the presence of decarboxylase genes (hdcA, tyrS, tyrDC, Odc, ldc) was detected by molecular assays, with the use of optimized primers enabling the detection of tyrDC in strains previously considered negative. The results showed high variability between strains and the ability of some isolates to produce high concentrations of tyrDC (max. > 1000 mg/kg); the presence of the tyrDC gene was strongly correlated with high production, although tyrDC-positive strains with low production were also reported, suggesting the influence of regulatory or environmental factors. The study underscores the need for precise molecular tools and systematic monitoring of biogenic amines to ensure the safety and quality of dairy products.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/ijms262110480

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 70

  1. Bohrer, 2017, Review: Nutrient Density and Nutritional Value of Meat Products and Non-Meat Foods High in Protein, Trends Food Sci. Technol., 65, 103, 10.1016/j.tifs.2017.04.016 · DOI · Paper page
  2. Zwietering, 2016, Relevance of Microbial Finished Product Testing in Food Safety Management, Food Control, 60, 31, 10.1016/j.foodcont.2015.07.002 · DOI
  3. Barlow, 2015, The Role of Hazard- and Risk-Based Approaches in Ensuring Food Safety, Trends Food Sci. Technol., 46, 176, 10.1016/j.tifs.2015.10.007 · DOI
  4. Ruiz-Capillas, C., and Herrero, A. (2019). Impact of Biogenic Amines on Food Quality and Safety. Foods, 8. · DOI · Paper page
  5. Guo, 2015, Biogenic Amines in Wine: A Review, Int. J. Food Sci. Technol., 50, 1523, 10.1111/ijfs.12833 · DOI
  6. Kacar, 2015, Inhibition Effects of Carvacrol on Biogenic Amines Formation by Common Food-Borne Pathogens in Histidine Decarboxylase Broth, LWT, 64, 50, 10.1016/j.lwt.2015.05.027 · DOI
  7. Cunha, 2017, Biogenic Amines in Liqueurs: Influence of Processing and Composition, J. Food Compos. Anal., 56, 147, 10.1016/j.jfca.2016.11.016 · DOI
  8. 2014, Health Effects and Occurrence of Dietary Polyamines: A Review for the Period 2005–Mid 2013, Food Chem., 161, 27, 10.1016/j.foodchem.2014.03.102 · DOI
  9. Akyol, 2021, Accuracy and Uniformity of the Nomenclature of Biogenic Amines and Polyamines in Metabolomics Studies: A Preliminary Study, BMB, 49, 441
  10. Gloria, 2023, Health Concerns Associated with Biogenic Amines in Food and Interaction with Amine Oxidase Drugs, Curr. Opin. Food Sci., 54, 101090, 10.1016/j.cofs.2023.101090 · DOI
  11. Fernandez, 2024, New Insights into the Toxicological Effects of Dietary Biogenic Amines, Food Chem., 435, 137558, 10.1016/j.foodchem.2023.137558 · DOI
  12. Jeon, 2018, Biogenic Amine Formation and Bacterial Contribution in Cheonggukjang, a Korean Traditional Fermented Soybean Food, LWT, 92, 282, 10.1016/j.lwt.2018.02.047 · DOI
  13. Hu, M., Dong, J., Tan, G., Li, X., Zheng, Z., and Li, M. (2021). Metagenomic Insights into the Bacteria Responsible for Producing Biogenic Amines in Sufu. Food Microbiol., 98. · DOI · Paper page
  14. Kim, 2021, Identification of Biogenic Amine-Producing Microbes during Fermentation of Ganjang, a Korean Traditional Soy Sauce, through Metagenomic and Metatranscriptomic Analyses, Food Control, 121, 107681, 10.1016/j.foodcont.2020.107681 · DOI
  15. Ladero, 2015, Genetic and Functional Analysis of Biogenic Amine Production Capacity among Starter and Non-Starter Lactic Acid Bacteria Isolated from Artisanal Cheeses, Eur. Food Res. Technol., 241, 377, 10.1007/s00217-015-2469-z · DOI
  16. Lorenzo, 2017, Role of Autochthonous Starter Cultures in the Reduction of Biogenic Amines in Traditional Meat Products, Curr. Opin. Food Sci., 14, 61, 10.1016/j.cofs.2017.01.009 · DOI
  17. Ladero, 2012, Is the Production of the Biogenic Amines Tyramine and Putrescine a Species-Level Trait in Enterococci?, Food Microbiol., 30, 132, 10.1016/j.fm.2011.12.016 · DOI
  18. Graham, 2020, Safety, Beneficial and Technological Properties of Enterococci for Use in Functional Food Applications—A Review, Crit. Rev. Food Sci. Nutr., 60, 3836, 10.1080/10408398.2019.1709800 · DOI
  19. Almeida, 2017, Functional and Structural Characterization of Synthetic Cardosin B-Derived Rennet, Appl. Microbiol. Biotechnol., 101, 6951, 10.1007/s00253-017-8445-8 · DOI
  20. Nami, Y., Vaseghi Bakhshayesh, R., Mohammadzadeh Jalaly, H., Lotfi, H., Eslami, S., and Hejazi, M.A. (2019). Probiotic Properties of Enterococcus Isolated From Artisanal Dairy Products. Front. Microbiol., 10. · DOI
  21. Montanari, C., Barbieri, F., Lorenzini, S., Gottardi, D., Šimat, V., Özogul, F., Gardini, F., and Tabanelli, G. (2023). Survival, Growth, and Biogenic Amine Production of Enterococcus faecium FC12 in Response to Extracts and Essential Oils of Rubus Fruticosus and Juniperus Oxycedrus. Front. Nutr., 9. · DOI
  22. Suárez, C., Espariz, M., Blancato, V.S., and Magni, C. (2013). Expression of the Agmatine Deiminase Pathway in Enterococcus faecalis Is Activated by the AguR Regulator and Repressed by CcpA and PTSMan Systems. PLoS ONE, 8. · DOI
  23. Landete, 2010, The Role of Two Families of Bacterial Enzymes in Putrescine Synthesis from Agmatine via Agmatine Deiminase, Int. Microbiol., 13, 169
  24. Perez, M., Ladero, V., Del Rio, B., Redruello, B., De Jong, A., Kuipers, O., Kok, J., Martin, M.C., Fernandez, M., and Alvarez, M.A. (2017). The Relationship among Tyrosine Decarboxylase and Agmatine Deiminase Pathways in Enterococcus faecalis. Front. Microbiol., 8. · DOI · Paper page
  25. Wasik, 2017, Development and Validation of an LC–MS/MS Method for the Determination of Biogenic Amines in Wines and Beers, Monatsh. Chem., 148, 1685, 10.1007/s00706-017-1992-y · DOI
  26. Dapkevicius, M.D.L.E., Sgardioli, B., Câmara, S.P.A., Poeta, P., and Malcata, F.X. (2021). Current Trends of Enterococci in Dairy Products: A Comprehensive Review of Their Multiple Roles. Foods, 10. · DOI
  27. Hanzelová, Z., Dudriková, E., Lovayová, V., Výrostková, J., Regecová, I., Zigo, F., and Bartáková, K. (2024). Occurrence of Enterococci in the Process of Artisanal Cheesemaking and Their Antimicrobial Resistance. Life, 14. · DOI
  28. Sarantinopoulos, 2001, Biochemical Properties of Enterococci Relevant to Their Technological Performance, Int. Dairy J., 11, 621, 10.1016/S0958-6946(01)00087-5 · DOI
  29. Nasiri, 2022, Enterococcus faecalis and Enterococcus faecium in Pasteurized Milk: Prevalence, Genotyping, and Characterization of Virulence Traits, LWT, 153, 112452, 10.1016/j.lwt.2021.112452 · DOI
  30. Bover-Cid, S., Latorre-Moratalla, M.L., Veciana-Nogués, M.T., and Vidal-Carou, M.C. (2014). Processing Contaminants: Biogenic Amines. Encyclopedia of Food Safety, Elsevier. · DOI
  31. Smith, 2023, Rethinking, Reducing, and Refining the Classical Oral Tyramine Challenge Test of Monoamine Oxidase (MAO) Inhibitors, Clin. Transl. Sci., 16, 2058, 10.1111/cts.13612 · DOI
  32. Saad, B., and Tofalo, R. (2019). Chapter 1. Biogenic Amines Formation, Toxicity, Regulations in Food. Food Chemistry, Function and Analysis, Royal Society of Chemistry. · DOI
  33. Sadighara, 2024, Tyramine, a Biogenic Agent in Cheese: Amount and Factors Affecting Its Formation, a Systematic Review, Food Prod. Process. Nutr., 6, 30, 10.1186/s43014-024-00223-x · DOI
  34. Perez, M., Calles-Enríquez, M., Del Rio, B., Redruello, B., De Jong, A., Kuipers, O.P., Kok, J., Martin, M.C., Ladero, V., and Fernandez, M. (2019). Construction and Characterization of a Double Mutant of Enterococcus faecalis That Does Not Produce Biogenic Amines. Sci. Rep., 9. · DOI
  35. Jiménez, E., Ladero, V., Chico, I., Maldonado-Barragán, A., López, M., Martín, V., Fernández, L., Fernández, M., Álvarez, M.A., and Torres, C. (2013). Antibiotic Resistance, Virulence Determinants and Production of Biogenic Amines among Enterococci from Ovine, Feline, Canine, Porcine and Human Milk. BMC Microbiol., 13. · DOI
  36. Bargossi, 2017, Growth, Biogenic Amine Production and tyrDC Transcription of Enterococcus faecalis in Synthetic Medium Containing Defined Amino Acid Concentrations, J. Appl. Microbiol., 122, 1078, 10.1111/jam.13406 · DOI · Paper page
  37. Amuasi, G.R., Dsani, E., Owusu-Nyantakyi, C., Owusu, F.A., Mohktar, Q., Nilsson, P., Adu, B., Hendriksen, R.S., and Egyir, B. (2023). Enterococcus Species: Insights into Antimicrobial Resistance and Whole-Genome Features of Isolates Recovered from Livestock and Raw Meat in Ghana. Front. Microbiol., 14. · DOI
  38. Yerlikaya, 2019, Potential Use of Probiotic Enterococcus faecium and Enterococcus durans Strains in Izmir Tulum Cheese as Adjunct Culture, J. Food Sci. Technol., 56, 2175, 10.1007/s13197-019-03699-5 · DOI
  39. Silvetti, 2019, Does Enterococcus faecalis from Traditional Raw Milk Cheeses Serve as a Reservoir of Antibiotic Resistance and Pathogenic Traits?, FPD, 16, fpd.2018.2542
  40. Klementová, L., Purevdorj, K., Butor, I., Jančová, P., Bábková, D., Buňka, F., and Buňková, L. (2024). Reduction of Histamine, Putrescine and Cadaverine by the Bacteria Lacticaseibacillus casei Depending on Selected Factors in the Real Condition of the Dairy Product. Food Microbiol., 117. · DOI
  41. Suzzi, 2003, Biogenic Amines in Dry Fermented Sausages: A Review, Int. J. Food Microbiol., 88, 41, 10.1016/S0168-1605(03)00080-1 · DOI · Paper page
  42. Tuncer, 2013, Safety Assessment of Enterococcus faecium and Enterococcus faecalis Strains Isolated from Turkish Tulum Cheese, J. Food Saf., 33, 369, 10.1111/jfs.12061 · DOI
  43. Bargossi, E., Tabanelli, G., Montanari, C., Lanciotti, R., Gatto, V., Gardini, F., and Torriani, S. (2015). Tyrosine Decarboxylase Activity of Enterococci Grown in Media with Different Nutritional Potential: Tyramine and 2-Phenylethylamine Accumulation and tyrDC Gene Expression. Front. Microbiol., 6. · DOI
  44. Eom, 2015, Biogenic Amine Degradation by Bacillus Species Isolated from Traditional Fermented Soybean Food and Detection of Decarboxylase-Related Genes, J. Microbiol. Biotechnol., 25, 1519, 10.4014/jmb.1506.06006 · DOI
  45. Lucas, 2003, The Tyrosine Decarboxylase Operon of Lactobacillus brevis IOEB 9809: Characterization and Conservation in Tyramine-Producing Bacteria, FEMS Microbiol. Lett., 229, 65, 10.1016/S0378-1097(03)00787-0 · DOI · Paper page
  46. Perez, 2015, Tyramine Biosynthesis Is Transcriptionally Induced at Low pH and Improves the Fitness of Enterococcus faecalis in Acidic Environments, Appl. Microbiol. Biotechnol., 99, 3547, 10.1007/s00253-014-6301-7 · DOI · Paper page
  47. Park, Y.K., Jin, Y.H., Lee, J.-H., Byun, B.Y., Lee, J., Jeong, K.C., and Mah, J.-H. (2020). The Role of Enterococcus faecium as a Key Producer and Fermentation Condition as an Influencing Factor in Tyramine Accumulation in Cheonggukjang. Foods, 9. · DOI
  48. Liu, 2015, Effect of NaCI Treatments on Tyramine Biosynthesis of Enterococcus faecalis, J. Food Prot., 78, 940, 10.4315/0362-028X.JFP-14-443 · DOI
  49. Marcobal, 2012, Tyramine and Phenylethylamine Biosynthesis by Food Bacteria, Crit. Rev. Food Sci. Nutr., 52, 448, 10.1080/10408398.2010.500545 · DOI
  50. Linares, 2004, Sequencing of the Tyrosine Decarboxylase Cluster of Lactococcus lactis IPLA 655 and the Development of a PCR Method for Detecting Tyrosine Decarboxylating Lactic Acid Bacteria, J. Food Prot., 67, 2521, 10.4315/0362-028X-67.11.2521 · DOI
  51. Bonham, 2017, Extensive Horizontal Gene Transfer in Cheese-Associated Bacteria, eLife, 6, e22144, 10.7554/eLife.22144 · DOI
  52. Vinayamohan, 2022, Role of Horizontal Gene Transfer in the Dissemination of Antimicrobial Resistance in Food Animal Production, Curr. Opin. Food Sci., 47, 100882, 10.1016/j.cofs.2022.100882 · DOI
  53. Bhardwaj, 2009, Tyramine-Producing Enterococci Are Equally Detected on Tyramine Production Medium, by Quantification of Tyramine by HPLC, or by Tdc Gene-Targeted PCR, Dairy Sci. Technol., 89, 601, 10.1051/dst/2009040 · DOI
  54. 2009, Production of Biogenic Amines by Enterococci, Czech J. Food Sci., 27, SII50, 10.17221/673-CJFS · DOI
  55. Kalhotka, 2012, Decarboxylase Activity Test of the Genus Enterococcus Isolated from Goat Milk and Cheese, Acta Vet. Brno, 81, 145, 10.2754/avb201281020145 · DOI
  56. Linares, 2006, Real-Time Polymerase Chain Reaction for Quantitative Detection of Histamine-Producing Bacteria: Use in Cheese Production, J. Dairy Sci., 89, 3763, 10.3168/jds.S0022-0302(06)72417-1 · DOI
  57. Coton, 2004, Identification of the Gene Encoding a Putative Tyrosine Decarboxylase of Carnobacterium Divergens 508. Development of Molecular Tools for the Detection of Tyramine-Producing Bacteria, Food Microbiol., 21, 125, 10.1016/j.fm.2003.10.004 · DOI
  58. Torriani, 2008, Rapid Detection and Quantification of Tyrosine Decarboxylase Gene (Tdc) and Its Expression in Gram-Positive Bacteria Associated with Fermented Foods Using PCR-Based Methods, J. Food Prot., 71, 93, 10.4315/0362-028X-71.1.93 · DOI
  59. Bargossi, E., Gardini, F., Gatto, V., Montanari, C., Torriani, S., and Tabanelli, G. (2015). The Capability of Tyramine Production and Correlation between Phenotypic and Genetic Characteristics of Enterococcus faecium and Enterococcus faecalis Strains. Front. Microbiol., 6. · DOI · Paper page
  60. Elsanhoty, 2016, Genetic Screening of Biogenic Amines Production Capacity from Some Lactic Acid Bacteria Strains, Food Control, 68, 220, 10.1016/j.foodcont.2016.04.002 · DOI
  61. Landete, 2007, Molecular Methods for the Detection of Biogenic Amine-Producing Bacteria on Foods, Int. J. Food Microbiol., 117, 258, 10.1016/j.ijfoodmicro.2007.05.001 · DOI
  62. Zarzecka, U., Zadernowska, A., and Chajęcka-Wierzchowska, W. (2022). Effects of Osmotic and High Pressure Stress on Expression of Virulence Factors among Enterococcus spp. Isolated from Food of Animal Origin. Food Microbiol., 102. · DOI
  63. Wiśniewski, P., Zakrzewski, A.J., Zadernowska, A., and Chajęcka-Wierzchowska, W. (2022). Antimicrobial Resistance and Virulence Characterization of Listeria monocytogenes Strains Isolated from Food and Food Processing Environments. Pathogens, 11. · DOI
  64. Zakrzewski, A.J., Zarzecka, U., Chajęcka-Wierzchowska, W., and Zadernowska, A. (2022). A Comparison of Methods for Identifying Enterobacterales Isolates from Fish and Prawns. Pathogens, 11. · DOI
  65. Zarzecka, 2022, Microorganisms from Starter and Protective Cultures—Occurrence of Antibiotic Resistance and Conjugal Transfer of Tet Genes in Vitro and during Food Fermentation, LWT, 153, 112490, 10.1016/j.lwt.2021.112490 · DOI
  66. Wiśniewski, P., Zakrzewski, A., Chajęcka-Wierzchowska, W., and Zadernowska, A. (2024). Possibility of Transfer and Activation of “silent” Tetracycline Resistance Genes among Enterococcus faecalis under High-Pressure Processing. Food Microbiol., 120. · DOI
  67. Holzapfel, 1999, Improved Screening Procedure for Biogenic Amine Production by Lactic Acid Bacteria, Int. J. Food Microbiol., 53, 33, 10.1016/S0168-1605(99)00152-X · DOI
  68. Barbieri, F., Tabanelli, G., Montanari, C., Dall’Osso, N., Šimat, V., Smole Možina, S., Baños, A., Özogul, F., Bassi, D., and Fontana, C. (2021). Mediterranean Spontaneously Fermented Sausages: Spotlight on Microbiological and Quality Features to Exploit Their Bacterial Biodiversity. Foods, 10. · DOI
  69. Martuscelli, 2000, Biogenic Amine Formation and Oxidation by Staphylococcus xylosus Strains from Artisanal Fermented Sausages, Lett. Appl. Microbiol., 31, 228, 10.1046/j.1365-2672.2000.00796.x · DOI
  70. Li, L., Wen, X., Wen, Z., Chen, S., Wang, L., and Wei, X. (2018). Evaluation of the Biogenic Amines Formation and Degradation Abilities of Lactobacillus curvatus From Chinese Bacon. Front. Microbiol., 9. · DOI

Metadata

Authors
Wiśniewski, P., & Barbieri, F.
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2025-10-28
Volume
26
Issue
21
Pages
10480
ISSN
1422-0067
DOI
10.3390/ijms262110480
Cited by
1
References
2
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.