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Studies on the Biogenic Amines Produced During Fermentation, Toxicity, and Techniques in Cereal Based Fermented Foods

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Sustainable Food Systems (Volume II)

Part of the book series: World Sustainability Series ((WSUSE))

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Abstract

Recent developments in food security and quality have prompted a greater search for trace substances that can affect human health and health agencies worldwide. Food poisoning has become more common as a result of our modern lifestyle and market globalization. Foodborne sickness and food poisoning can be caused by a variety of organisms (bacteria, viruses, parasites, mould, pollutants, and so on), and certain cases of food poisoning can be traced back to chemical and natural toxins. The biogenic amine is one of the toxic compounds addressed by the Food and Drug Administration (FDA) and the European Food Safety Authority (EFSA). These Biogenic amines are natural amines and anti-nutritional factors, constitute a potential public health concern due to their toxicological effects. Their concentrations typically rise when food is subjected to regulated or uncontrolled microbial fermentation or when food deteriorates. The consumption of foods containing high concentrations of biogenic amines has been associated with health hazards. Cereal grains constitute a major source of dietary nutrients all over the world. Cereal grains are an important source of healthy nutrients all around the world. Although cereals are deficient in some basic components (e.g. essential aminoacids), fermentation may be the most simple and economical way of improving their nutritional value, sensory properties, and functional qualities. Lactic acid bacteria (LAB) are usually considered to be non-toxic and non-pathogenic but some LAB species, however, can generate biogenic amines, although the levels are below the of toxicity limit. Biogenic amines are found in a wide variety of cereal-based fermented foods (rice, wheat, corn, cereals, soya bean, etc.), and biogenic amine formation is regulated by various factors related to the raw material used to make food products, microbes, processing, and storage conditions. Biogenic amines are also essential markers of food quality and/or acceptance. These biogenic amines can be quantified using analytical methods that are mostly based on chromatographic procedures. Hence, biogenic amines must be monitored in food to maintain the standard of quality of food and safety. This review will highlight the importance of biogenic amines in cereal foods.

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References

  • Al Bulushi I, Poole S, Deeth HC, Dykes GA (2009) Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation—A review. Crit Rev Food Sci Nutr 49:369–377

    Article  CAS  PubMed  Google Scholar 

  • Arena ME, Landete JM, Manca de Nadra MC, Pardo I, Ferrer S (2008) Factors affecting the production of putrescine from agmatine by Lactobacillus hilgardii XB isolated from wine. J Appl Microbiol 105(1):158–165. https://doi.org/10.1111/j.1365-2672.2008.03725.x

  • Alvarez MA, Moreno-Arribas MV (2014) The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trend Food Sci Technol 39:146–155

    Article  CAS  Google Scholar 

  • Askar A, Treptow H (1986) Biogene Amine in Lebensmitteln: Vorkommen, Bedeutung and Bestimmung. E. Ulmer, Stuttgart, Germany

    Google Scholar 

  • Battcock M, Azam-Ali S (1998) Fermented fruits and vegetables: a global perspective

    Google Scholar 

  • Berbegal C, Pardo I, Ferrer S (2016) The use of core-shell high performance liquid chromatography column technology to improve the biogenic amine quantification in wine. J Sci Food Agric 2016(96):1556–1561

    Article  Google Scholar 

  • Bodmer S, Imark C, M Kneubühl (1999) Biogenic amines in foods: histamine and food processing. Inflamm Res 48:296–300

    Google Scholar 

  • Bardócz S (1995) Polyamines in food and their consequences for food quality and human health. Trends Food Sci Technol 6:341–346

    Article  Google Scholar 

  • Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33–41

    Article  CAS  PubMed  Google Scholar 

  • Cho TY, Han GH, Bahn KN, Son YW, Jang MR, Lee CH, Kim SH, Kim DB, Kim SB (2006) Evaluation of biogenic amines in Korean commercial fermented foods. Korean J Food Sci Technol 38(6):730–737.

    Google Scholar 

  • Chou CC, Ling MY (1998) Biochemical changes in soy sauce prepared with extruded and traditional raw materials. Food Res Int 31:487–492

    Article  CAS  Google Scholar 

  • Collins JD, Noerrung B, Budka H et al (2011) Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA J 9:2393

    Article  Google Scholar 

  • Cosansu S (2009) Determination of biogenic amines in a fermented beverage, boza. J Food Agri Environ 7(2):54–58

    CAS  Google Scholar 

  • Coton E, Coton M (2005) Multiplex PCR for colony direct detection of gram positive histamine- and tyramine-producing bacteria. J Microbiol Method 63:296–304

    Google Scholar 

  • De Mey E, De Klerck K, De Maere H, Dewulf L, Derdelinckx G, Peeters MC, Fraeye I, Vander Heyden Y, Paelinck H (2014) The occurrence of N-nitrosamines, residual nitrite and biogenic amines in commercial dry fermented sausages and evaluation of their occasional relation. Meat Sci 96:821–828

    Article  PubMed  Google Scholar 

  • Dimidi E, Cox SR, Rossi M, Whelan K (2019) Fermented foods: definitions and characteristics, impact on the gut microbiota and effects on gastrointestinal health and disease. Nutrien 11(8):1806. https://doi.org/10.3390/nu11081806

    Article  CAS  Google Scholar 

  • Eerola S, Maijala R, Roig-Sague´s AX, Salminen M, Hirvi TK (1998a). Biogenic amines in dry sausages as affected by starter culture and contaminant amine-positive Lactobacillus. J Food Sci 61:1243–1246.

    Google Scholar 

  • EFSA (2007) Opinion of the scientific committee related to uncertainties in dietary exposure assessment. EFSA J 5(1):438

    Google Scholar 

  • EFSA (2011) Scientific Opinion on risk based control of biogenic amine formation in fermented foods. EFSA J 9:2393

    Article  Google Scholar 

  • Fernandez M, Linares DM, Rodriguez A, Alvarez MA (2007) Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl Microbiol Biotechnol 73(6):1400–1406. https://doi.org/10.1007/s00253-006-0596-yW.N

    Article  CAS  PubMed  Google Scholar 

  • Fong FL, Lam KY, San Lau C, Ho KH, Kan YH, Poon MY, El-Nezami H, Sze ET(2020) Reduction in biogenic amines in douchi fermented by probiotic bacteria. PLoS One 15(3)

    Google Scholar 

  • Ekinci R, Kadakal C (2005) Determination of seven water-soluble vitamins in tarhana, a traditional Turkish cereal food, by high-performance liquid chromatography. ACTA Chromatogr 15:289

    CAS  Google Scholar 

  • Guan RF, Liu ZF, Zhang JJ, Wei YX, Wahab S, Liu DH, Ye XQ (2013) Investigation of biogenic amines in sufu (furu): a Chinese traditional fermented soybean food product. Food Control 31(2):345–352 (FAO Agricultural Services Bulletin, Vialedelle Terme di Caracalla 00100). https://doi.org/10.1016/j.foodcont.2012.10.033.Rome

  • Gardini F, Özogul Y, Suzzi G, Tabanelli G, Özogul F (2016) Technological factors affecting biogenic amine content in foods: a review. Frontiers Microbiol 7, 1218.

    Google Scholar 

  • Ghosh D, Chattopadhyay P (2011) Preparation of idli batter, its properties and nutritional improvement during fermentation. J Food Sci Technol 48:610–615

    Article  CAS  PubMed  Google Scholar 

  • Griswold AR, Jameson-Lee M, Burne RA (2006) Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol 188(3):834–841. https://doi.org/10.1128/JB.188.3.834-841.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halasz A, Barath A, Simon-Sarkadi L, Holzapfel W (1994) Biogenic-amines and their production by microorganisms in food. Trend Food Sci Technol 5:42–49

    Article  CAS  Google Scholar 

  • Hernandez-Cassou S, Saurina J (2013) Determination of histamine in wine samples by flow-injection analysis and multivariate calibration. Anal Lett 46:1758−1768

    Google Scholar 

  • Hernandez-Jover T, Izquierdo-Pulido M, Veciana-Nogues MT, Marine-Font A, Vidal-Carou MC (1997) Biogenic amines and polyamine contents in meat and meat products. J Agri Food Chem 45:2098–2102

    Article  CAS  Google Scholar 

  • Hutkins RW (2006) Microbiology and technology of fermented foods. IFT, Iowa, p 473

    Google Scholar 

  • Ibanoglu S, Ainsworth P, Wilson G, Hayes GD (1995) Effect of formulation on protein breakdown, in vitro digestibility, rheological properties and acceptability of tarhana, a traditional Turkish cereal food. Int. J Food Sci Technol 30(5):579–585

    Article  CAS  Google Scholar 

  • Jia S, Kang YP, Park JH, Lee J, Kwon SW (2012) Determination of biogenic amines in Bokbunja (Rubuscoreanus Miq.) wines using a novel ultra-performance liquid chromatography coupled with quadrupole-time of flight mass spectrometry. Food Chem 132:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Kalac P (2014) Health effects and occurrence of dietary polyamines: a review for the period 2005-mid. Food Chem 161:27–39. https://doi.org/10.1016/j.FoodChem2014.03.102

    Article  CAS  PubMed  Google Scholar 

  • Kim MK, Mah JH, Hwang HJ (2009) Biogenic amine formation and bacterial contribution in fish, squid and shellfish. Food Chem 116:87–95

    Article  CAS  Google Scholar 

  • Kleerebezem M, Boekhorst J, Van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci 100:1990–1995

    Google Scholar 

  • Kvasnicka F, Voldrich M (2006) Determination of biogenic amines by capillary zone electrophoresis with conductometric detection. J Chromat A 1103:145–149

    Article  CAS  Google Scholar 

  • Ladero VM, Linares DM, Fernández M, Alvarez MA (2008). Real time quantitative PCR detection of histamine-producing lactic acid bacteria in cheese: relation with histamine content. Food Res Int 41:1015–1019

    Google Scholar 

  • Latorre-Moratalla ML, Comas-Baste O, Bover-Cid S, Vidal-Carou MC (2017) Tyramine and histamine risk assessment related to consumption of dry fermented sausages by the Spanish population. Food Chem Toxicol 99:78–85. https://doi.org/10.1016/j.fct.2016.11.011

    Article  CAS  PubMed  Google Scholar 

  • Linares DM, Cruz Martín M, Ladero V, Alvarez MA, Fernandez M (2011) Biogenic amines in dairy products. Critical Rev Food Sci Nutr 51(7):691-703

    Google Scholar 

  • Liu Q, Wu J, Lim ZY, Aggarwal A, Yang H, Wang S (2017) Evaluation of the metabolic response of Escherichia coli to electrolysed water by 1H NMR spectroscopy. LWT 79:428–436

    Google Scholar 

  • Liu Q, Wu J, Lim ZY, Lai S, Lee N, Yang H (2018) Metabolite profiling of Listeria innocua for unravelling the inactivation mechanism of electrolysed water by nuclear magnetic resonance spectroscopy. Int J Food Microbiol 271:24–32

    Article  PubMed  Google Scholar 

  • Lucas PM, Claisse O, Lonvaud-Funel A (2008) High frequency of histamine producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl Environ Microbiol 74:811–817

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Huang Y, Xu R, Qian B, Zhou J, Xia X (2020) Primary and secondary succession mediates the accumulation of biogenic amines during industrial semidry Chinese rice wine fermentation. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01177-20.AEM.01177-20

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcobal A, De las Rivas B, Muñoz R (2006) Methods for the detection of bacteria producing biogenic amines on foods: a survey. J Con Prot Food Safety 1:187–196

    Google Scholar 

  • Mariné-Font A, Vidal-Carou C, Izquierdo-Pulido M, Veciana-Nogués T, Hernández-Jover T (1995) Les amines biogenes dans les aliments: leur signification, leur analyse. Annalesdeus Falsifications, de l’Expertise Chimique et Toxicologique 88:119–140

    Google Scholar 

  • Melnikov M, Rogovskii V, Boyko A, Pashenkov M (2018) The influence of biogenic amines on Th17-mediated immune response in multiple sclerosis. Multiple Sclero Rel Disord 21:19–23. https://doi.org/10.1016/j.msard.2018.02.012

    Article  Google Scholar 

  • Mitacek EJ, Brunnemann KD, Suttajit M, Martin N, Limsila T, Ohshima H et al (1999) Exposure to N-nitroso compounds in a population of high liver cancer regions in Thailand: volatile nitrosamine (VNA) levels in Thai food. Food Chem Toxicol 37(4):297–305

    Article  CAS  PubMed  Google Scholar 

  • Nalazek-Rudnicka K, Wojnowski W, Wasik A (2021) Occurrence and levels of biogenic amines in beers produced by different methods. Food 10(12):2902

    Article  CAS  Google Scholar 

  • Nannelli F, Claisse O, Gindreau E, de Revel G, Lonvaud-Funel A, Lucas PM (2008) Determination of lactic acid bacteria producing biogenic amines in wine by quantitative PCR methods. Lett Appl Microbiol 47:594–599

    Article  CAS  PubMed  Google Scholar 

  • Nout MJR (1994) Fermented foods and food safety. Food Res Int 27:291–298

    Article  CAS  Google Scholar 

  • Nyarko-mensah B, Muller HG (1972) Studies on kenkey, a Ghanaian cereal food. J Sci Food Agri 23:544–545

    Article  Google Scholar 

  • Onal A (2007) A review: Current analytical methods for the determination of biogenic amines in foods. Food Chem 103:1475–1486

    Article  Google Scholar 

  • Onal A, Tekkeli SEK, Onal C (2013) A review of the liquid chromatographic methods for the determination of biogenic amines in foods. Food Chem 138:509–515

    Article  CAS  PubMed  Google Scholar 

  • Özdestan Ö et al (2012) Monitoring of biogenic amines in Kumru: a traditional fermented cereal food. Int J Food Prop 15(5):972–981

    Article  Google Scholar 

  • Ozogul F, Hamed I (2018) The importance of lactic acid bacteria for the prevention of bacterial growth and their biogenic amines formation: a review. Crit Rev Food Sci Nutr 58(10):1660–1670. https://doi.org/10.1080/10408398.2016.1277972

    Article  CAS  PubMed  Google Scholar 

  • Padhye VW, Salunkhe DK (1979) Biochemical studies on black gram (Phaseolus mungo L.) seeds: amino acid composition and subunit constitution of fractions of the proteins. J Food Sci 44(2):606–614

    Google Scholar 

  • Parente E, Matuscelli M, Gadrini F, Grieco S, Crudele MA, Suzzi G (2001) Evolution of microbial populations and biogenic amines production in dry sausages produced in southern Italy. J Appl Microbiol 90:882–891

    Article  CAS  PubMed  Google Scholar 

  • Pegg AE (2013) Toxicity of polyamines and their metabolic products. Chem Res Toxicol 26:1782–2180

    Article  CAS  PubMed  Google Scholar 

  • Perez M, Calles-Enríquez M, Nes I, Martin MC, Fernandez M, Ladero V, Alvarez MA (2015) Tyramine biosynthesis is transcriptionally induced at low pH and improves the fitness of Enterococcus faecalisin acidic environments. Appl Microbiol Biotechnol 99:3547–3558. https://doi.org/10.1007/s00253-014-6301-7

  • Poveda JM (2019) Biogenic amines and free amino acids in craft beers from the Spanish market: a statistical approach. Food Control 96:227–33.

    Google Scholar 

  • Regubalan B, Ananthanarayan L (2019) Investigation of biogenic amines content in fermented idli batter during storage. J Food Sci Technol 56:1775–1784

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Capillas C, Jiménez-Colmenero F (2004) Biogenic amines in meat and meat products. Crit Rev Food Sci Nutr 44:489–499

    Article  CAS  PubMed  Google Scholar 

  • Sahu L, Panda SK, Paramithiotis S, Zdolec N, Ray RC (2015) Biogenic amines in fermented foods: overview. In: Montet D, Ramesh CR (eds) Fermented foods—Part I: biochemistry and biotechnology. CRC Press, Boca Raton, FL, USA, pp 318–332

    Google Scholar 

  • Santos MS (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29(2–3):213–231

    Article  CAS  Google Scholar 

  • Schwenke KD, Askar A, Treptow H (1986) Biogene Amine in Lebensmitteln—Vorkommen, Bedeutung and Bestimmung. 197 Seiten, 34 Abb., 47 Tab. VerlagEugen Ulmer. Stuttgart. Preis: 58, DM. Mol Nutr Food Res 32(4) (2010):420. https://doi.org/10.1002/food.19880320433

  • Schneiderbanger J, Jacob F, Hutzler M (2020) Mini-review: the current role of lactic acid bacteria in beer spoilage. Mon Für Brauwissen 73:2

    Google Scholar 

  • Self RL, Wu WH (2012) Determination of eight biogenic amines in selected seafood products by MSPD extraction followed by UHPLC Orbitrap MS. J Food Compos Anal 27:169–173

    Article  CAS  Google Scholar 

  • Self RL, Wu WH, Marks HS (2011) Simultaneous quantification of eight biogenic amine compounds in tuna by matrix solid-phase dispersion followed by HPLC-Orbitrap mass spectrometry. J Agric Food Chem 59:5906–5913

    Article  CAS  PubMed  Google Scholar 

  • Shalaby AR (1996) Significance of biogenic amines to food safety and human health. Food Res Int 29:675–690

    Article  CAS  Google Scholar 

  • Shalaby AR (1999) Simple, rapid and valid thin layer chromatographic method for determining biogenic amines in foods. Food Chem 65(1):117-21

    Google Scholar 

  • Stadnik J, Dolatowski ZJ (2010) Biogenic amines in meat and fermented meat products. Acta Sci Pol Technol Aliment 9:251–263

    CAS  Google Scholar 

  • Stute R, Petridis K, Steinhart H, Biernoth G (2002) Biogenic amines in fish and soy sauces. Euro Food Res Technol 215:101–107

    Article  CAS  Google Scholar 

  • Suzzi G, Gardini F (2003) Biogenic amines in dry fermented sausages: a review. Int J Food Microbiol 88:41–54

    Article  CAS  PubMed  Google Scholar 

  • Tabanelli G, Torriani S, Rossi F, Rizzotti L, Gardini F (2012) Effect of chemico‐physical parameters on the histidine decarboxylase (HdcA) enzymatic activity in Streptococcus thermophilus PRI60. J Food Sci 77(4):231–237.

    Google Scholar 

  • Tamer CE, Kumral A, Asan M, Sahin I (2007) Chemical compositions of traditional tarhana having different formulations. J Food Process Preser 31(1):116–126

    Article  CAS  Google Scholar 

  • Taylor SL (1985) World Health Organization. Histamine poisoning associated with fish, cheese, and other foods. World Health Organization.

    Google Scholar 

  • Thomas K, Wittmann C (2003) Comparison of a capillary electrophoresis method with high-performance liquid chromatography for the determination of biogenic amines in various food samples. J Chromat B: Analytechnol Biomed Life Sci 779:229–239

    Google Scholar 

  • Tsai Y-H et al (2007) Histamine formation by histamine-forming bacteria in douchi, a Chinese traditional fermented soybean product. Food Chem 103(4):1305–1311

    Article  CAS  Google Scholar 

  • Veciana-Nogués MT, Mariné-Font A, Vidal-Carou MC (1997) Biogenic amines as hygienic quality indicators of tuna. Relationships with microbial counts, ATP-related compounds, volatile amines, and organoleptic changes. J Agri Food Chem 45(6), 2036–2041

    Google Scholar 

  • Walters MJ (1984) Determination of histamine in fish by liquid chromatography with post-column reaction and fluorometric detection. J AOAC 67(6):1040–1043.

    Google Scholar 

  • Yeğin S, Üren A (2008) Biogenic amine content of boza: a traditional cereal-based, fermented Turkish beverage. Food Chem 111(4):983–987

    Article  Google Scholar 

  • Yokotsuka T (1986) Soy sauce biochemistry. Adv Food Res 30:195–329

    Google Scholar 

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Authors and Affiliations

  1. Microbiology and Fermentation Technology Department, CSIR-Central Food Technological Research Institute, Mysuru, Karnataka, 570020, India

    S. Rohini Karnat, Simran Dubey & D. Somashekar

  2. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, 201002, India

    S. Rohini Karnat & D. Somashekar

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  1. S. Rohini Karnat
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  2. Simran Dubey
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Correspondence to D. Somashekar .

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  1. Amity Institute of Food Technology, Amity University, Noida, Uttar Pradesh, India

    Monika Thakur

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Karnat, S.R., Dubey, S., Somashekar, D. (2024). Studies on the Biogenic Amines Produced During Fermentation, Toxicity, and Techniques in Cereal Based Fermented Foods. In: Thakur, M. (eds) Sustainable Food Systems (Volume II). World Sustainability Series. Springer, Cham. https://doi.org/10.1007/978-3-031-46046-3_14

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