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Dietary exposure assessment of putrescine and cadaverine and derivation of tolerable levels in selected foods consumed in Austria

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Abstract

Biogenic amines (histamine, tyramine, putrescine, cadaverine, agmatine, spermidine and spermine) are nitrogenous compounds. They occur naturally in living organisms and are involved in many biological processes. Nonetheless, high amounts in food may be hazardous to human health. The diamines putrescine and cadaverine in food can potentiate the effects of simultaneously ingested histamine. In protein-rich foods, high concentrations of these diamines are indicative for hygienic deficiencies in the food chain. Even though being formed endogenously and being essential for some physiological metabolic pathways, both diamines are known as precursors for carcinogenic nitrosamines. Putrescine also plays a certain role in tumour growth. Nevertheless, no tolerable levels in foods have been established so far. The present study suggests tolerable levels in cheese, fermented sausages, fish, sauerkraut and seasonings that are based on toxicological threshold levels, occurrence of diamines in foods and food consumption in Austria. Average daily intake of putrescine via fermented food was calculated to be 6.8 (female adults) and 8.8 (male adults) mg per person. Respective numbers for cadaverine were 9.8 and 11.6 mg per person and day. For putrescine, proposed maximum tolerable levels for sauerkraut, fish, cheese, fermented sausages and seasonings are 140, 170, 180, 360 and 510 mg/kg, respectively. Likewise, for cadaverine, in sauerkraut, fish, cheese, fermented sausages and seasonings, maximum tolerable levels are 430, 510, 540, 1,080 and 1,540 mg/kg, respectively. These limits can be met by current manufacturing practices, as ascertained from the results of our own studies and from literature. Admittedly, only few data are published on toxicological threshold levels of these diamines, which mean that these tolerable levels are associated with some uncertainty.

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References

  1. Beutling DM (1996) Biogene Amine in der Ernährung. Springer, Wien

    Google Scholar 

  2. Silla-Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231

    Article  CAS  Google Scholar 

  3. Lehane L, Olley J (2000) Histamine fish poisoning revisited. Int J Food Microbiol 58:1–37

    Article  CAS  Google Scholar 

  4. Anderson KE (2010) Effects of specific foods and dietary components on drug metabolism—tyramine and related substances. In: Boullata JI, Armenti VT (eds) Handbook of drug–nutrient interactions, 2nd edn. Humana Press, New York

    Google Scholar 

  5. Ten Brink B, Damink C, Joosten HMLJ, Huis In’T Veld JHJ (1990) Occurrence and formation of biologically active amines in foods. Int J Food Microbiol 11:73–84

    Article  Google Scholar 

  6. Taylor SL (1986) Histamine food poisoning: toxicology and clinical aspects. CRC Crit Rev Toxicol 17:91–128

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Seiler N, Sarhan S, Grauffel C, Jones R, Knödgen B, Moulinoux JP (1990) Endogenous and exogenous polyamines in support of tumor growth. Cancer Res 50:5077–5083

    CAS  Google Scholar 

  9. Nebelin E, Pillai S, Lund E, Thomsen J (1980) On the formation of N-nitrosopyrrolidine from potential precursors and nitrite. IARC Sci Publ 31:183–193

    CAS  Google Scholar 

  10. European Commission (2005) Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Eur Union L 338:1–26

    Google Scholar 

  11. Food and Drug Administration (2011) Fish and fishery products hazards and controls guidance, 4th edn. FDA, Center for Food Safety and Applied Nutrition, Washington DC. http://www.fda.gov/downloads/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/Seafood/UCM251970.pdf. Accessed 10 April 2012

  12. Rauscher-Gabernig E, Grossgut R, Bauer F, Paulsen P (2009) Assessment of alimentary histamine exposure of consumers in Austria and development of tolerable levels in typical foods. Food Control 20:423–429

    Article  CAS  Google Scholar 

  13. Paulsen P, Grossgut R, Bauer F, Rauscher-Gabernig E (2012) Estimates of maximum tolerable levels of tyramine content in foods in Austria. J Food Res Nutr 51:52–59

    CAS  Google Scholar 

  14. Rauscher-Gabernig E, Grossgut R, Bauer F, Paulsen P (2010) Phenylethylamin in Lebensmitteln: Gehalte und Erarbeitung von tolerierbaren Höchstgehalten. Veterinary Med Austria 97:242–252

    CAS  Google Scholar 

  15. Codex Alimentarius Commission (1999) Principles and guidelines for the conduct of microbiological risk assessment—CAC/GL 30. http://www.codexalimentarius.net/download/standards/357/CXG_030e.pdf. Accessed 6 Dec 2011

  16. European Commission (2002) Commission Regulation (EC) No 178/2002 of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Official J Eur Union L 31:1–24

    Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Askar A, Treptow H (1986) Biogene Amine in Lebensmitteln: Vorkommen. Bedeutung und Bestimmung, Ulmer

    Google Scholar 

  19. Pircher A, Bauer F, Paulsen P (2007) Formation of cadaverine, histamine, putrescine and tyramine by bacteria isolated from meat, fermented sausages and cheeses. Eur Food Res Tech 226:225–231

    Article  CAS  Google Scholar 

  20. Kalac P (2009) Recent advances in the research on biological roles of dietary polyamines in man. J Appl Biomed 7:65–74

    CAS  Google Scholar 

  21. Milovic V, Odera G, Murphy GM, Dowling RH (1997) Jejunal putrescine absorption and the pharmacokinetics/biotransformation of ingested putrescine in humans. Gut 41:A62

    Google Scholar 

  22. Milovic V (2001) Polyamines in the gut lumen: bioavailability and biodistribution. Eur J Gastroenterol Hepatol 13:1021–1025

    Article  CAS  Google Scholar 

  23. Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233

    CAS  Google Scholar 

  24. Van den Berg GA, Muskiet FA, Kingma AW, Van der Slik W, Halie MR (1986) Simultaneous gas-chromatographic determination of free and acetyl-conjugated polyamines in urine. Clin Chem 32:1930–1937

    Google Scholar 

  25. Halasz A, Barath A (2002) In: Morgan DML, Hirvi T, Dandrifosse G, Deloyer P, White A (eds) COST 917: biogenically active amines in food, vol VI. EC Publication, Luxembourg

    Google Scholar 

  26. Hui JY, Taylor SL (1985) Inhibition of in vivo histamine metabolism in rats by foodborne and pharmacologic inhibitors of diamine oxidase, histamine N-methyltransferase, and monoamine oxidase. Toxicol Appl Pharmacol 81:241–249

    Article  CAS  Google Scholar 

  27. Chu CH, Bjeldanes LF (1981) Effect of diamines, polyamines and tuna fish extracts on the binding of histamine to mucin in vitro. J Food Sci 47(79–80):88

    Google Scholar 

  28. European Food Safety Authority (EFSA) (2011) Scientific Opinion on risk based control of biogenic amine formation in fermented foods. EFSA J 9(10):2393:1–93

    Google Scholar 

  29. Gerner EW, Meyskens FL Jr (2004) Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer 4:781–792

    Article  CAS  Google Scholar 

  30. Ladero V, Calles-Enriquez M, Fernandez M, Alvarez MA (2010) Toxicological effects of dietary biogenic amines. Curr Nutr Food Sci 6:145–156

    Article  CAS  Google Scholar 

  31. Schipper RG, Romijn JC, Cuijpers VM, Verhofstad AA (2003) Polyamines and prostatic cancer. Biochem Soc Trans 31:375–380

    Article  CAS  Google Scholar 

  32. Cipolla BG, Havouis R, Moulinoux JP (2007) Polyamine contents in current foods: a basis for polyamine reduced diet and a study of its long term observance and tolerance in prostate carcinoma patients. Amino Acids 33:203–212

    Article  CAS  Google Scholar 

  33. Cipolla BG, Havouis R, Moulinoux JP (2010) Polyamine reduced diet (PRD) nutrition therapy in hormone refractory prostate cancer patients. Biomed Pharmacother 64:363–368

    Article  CAS  Google Scholar 

  34. Til HP, Falke HE, Prinsen MK, Willems MI (1997) Acute and subacute toxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats. Food Chem Toxicol 35:337–348

    Article  CAS  Google Scholar 

  35. Verdam L, Krajnc E (1988) 1,4-butanediamine. RIVM Report 88/6788097003, adopted by the Toxicology Advisory. Group 03(05):1988

    Google Scholar 

  36. Official Collection of Methods—Amtliche Sammlung von Untersuchungsverfahren nach § 35 LMBG (1999) Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Berlin. http://www.methodensammlung-bvl.de/. Accessed 3 April 2012

  37. Elmadfa I, Freisling H, König J (2003) Österreichischer Ernährungsbericht 2003, 1st edn. Institute for Nutritional Science of the University of Vienna, Wien

    Google Scholar 

  38. Ibe A, Tamura Y, Kamimura H, Tabata S, Hashimoto H, Iida M, Nishima T (1991) Determination and contents of non-volatile amines in soybean paste and soy sauce. Eisei Kagaku 37:379–386

    Article  CAS  Google Scholar 

  39. Souci SW, Fachmann W, Kraut H (2000) Food composition and nutrition tables. Medpharm Scientific Publishers, Stuttgart

    Google Scholar 

  40. Bauer F, Paulsen P, Hagen U, Wasserbacher R, Elmadfa I, Ralph A, Bardocz S (2004) In: Wallace HM, Hughes H (eds) COST 922: health implications of dietary amines. EC publications, Luxembourg

    Google Scholar 

  41. Sakaguchi M, Murata M (1986) Distribution of free amino acids, creatine, and trimethylamine oxide in mackerel and yellowtail. Nippon Suisan Gakkai Shi 52:685–689

    Article  CAS  Google Scholar 

  42. 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  Google Scholar 

  43. Rabie M, Simon-Sarkadi L, Hassan S, El-seedy S, El Badawy AA (2009) Changes in free amino acids and biogenic amines of Egyptian salted-fermented fish (Feseekh) during ripening and storage. Food Chem 115:635–638

    Article  CAS  Google Scholar 

  44. Gingerich TM, Lorca T, Flick GJ, Pierson MD, McNair HM (1999) Biogenic amine survey and organoleptic changes in fresh, stored, and temperature-abused bluefish (Pomatomus saltatrix). J Food Prot 62:1033–1037

    CAS  Google Scholar 

  45. Jakob E, Badertscher R, Bütikofer U (2007) Zusammensetzung von Berner Alp- und Hobelkäse. AGRARForschung 14:96–101

    Google Scholar 

  46. Bütikofer U, Fuchs D (1997) Development of free amino acids in Appenzeller, Emmentaler, Gruyère, Raclette, Sbrinz and Tilsiter cheese. Lait 77:91–100

    Article  Google Scholar 

  47. Novella-Rodríguez S, Veciana-Nogues MT, Izquierdo-Pulido M, Vidal-Carou MC (2003) Distribution of biogenic amines and polyamines in cheese. J Food Sci 68:750–755

    Article  Google Scholar 

  48. Mayer HK, Fiechter G, Fischer E (2010) A new ultra-pressure liquid chromatography method for the determination of biogenic amines in cheese. J Chromatogr A 1217:3251–3257

    Article  CAS  Google Scholar 

  49. Eerola S, Maijala R, Roig-Sagues AX, Salminen M, Hirvi T (1996) Biogenic amines in dry sausages as affected by starter culture and contaminant amine-positive Lactobacillus. J Food Sci 61:1243–1246

    Article  CAS  Google Scholar 

  50. Simon-Sarkadi L (2005) In: Morgan DML, Bauer F, White A (eds) COST 917: biogenically active amines in food, vol VII. EC Publication, Luxembourg

    Google Scholar 

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

    Article  CAS  Google Scholar 

  52. Shukla S, Park HK, Kim JK, Kim M (2010) Determination of biogenic amines in Korean traditional fermented soybean paste (Doenjang). Food Chem Toxicol 48:1191–1195

    Article  CAS  Google Scholar 

  53. Pechanek U, Blaicher G, Pfannhauser W, Woidich H (1980) Beitrag zur Untersuchung biogener Amine in Käse und Fischen. Z Lebensm Unters Forsch 171:420–424

    Article  CAS  Google Scholar 

  54. Jae-Hyung M, Hyung-Kee H, Young-Jun O, Man-Goo K, Han-Joon H (2002) Biogenic amines in Jeotkals, Korean salted and fermented fish products. Food Chem 79:239–243

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  56. Spanjer MC, Van Roode BASW (1991) Towards a regulatory limit for biogenic amines in fish, cheese and sauerkraut. De Ware(n)-chemicus 21:139–167

    Google Scholar 

  57. Krizek M, Pavlicek T, Vacha F (2002) Formation of selected biogenic amines in carp meat. J Sci Food Agric 82:1088–1093

    Article  CAS  Google Scholar 

  58. Dawood AA, Karkalas J, Roy RN, Williams CS (1988) The occurrence of non-volatile amines in chilled-stored rainbow trout (Salmo irideus). Food Chem 27:33–45

    Article  CAS  Google Scholar 

  59. Yamanaka H, Shiomi K, Kikuchi T (1989) Cadaverine as a potential index for decomposition of salmonid fishes. J Food Hyg Soc Jpn 30:170–174

    Article  CAS  Google Scholar 

  60. Rezaei M, Montazeri N, Langrudi HE, Mokhayer B, Parviz M, Nazarinia A (2007) The biogenic amines and bacterial changes of farmed rainbow trout (Oncorhynchus mykiss) stored in ice. Food Chem 103:150–154

    Article  CAS  Google Scholar 

  61. Mietz JL, Karmas E (1977) Chemical quality index of canned tuna as determined by high-pressure liquid chromatography. J Food Sci 42:155–158

    Article  CAS  Google Scholar 

  62. Karmas E (1981) Biogenic amines as indicators of seafood freshness. Lebensm Wiss Technol 14:273–275

    CAS  Google Scholar 

  63. Bauer F, Paulsen P (2000) In: Gesellschaft Österreischischer Chemiker (eds) Österreichische Lebensmittelchemikertage, Organische Wirkstoffe in Lebensmitteln, Proceedings. Pörtschach

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Acknowledgments

The authors thank Frans J. M. Smulders for comment on the manuscript and language revision.

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Authors and Affiliations

  1. Data, Statistics and Risk Assessment, Austrian Agency for Health and Food Safety, Spargelfeldstrasse 191, 1220, Vienna, Austria

    Elke Rauscher-Gabernig, Werner Brueller & Roland Grossgut

  2. Institute for Food Safety Vienna, Austrian Agency for Health and Food Safety, Spargelfeldstrasse 191, 1220, Vienna, Austria

    Robert Gabernig

  3. Institute of Meat Hygiene, Meat Technology and Food Science in the Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210, Vienna, Austria

    Friedrich Bauer & Peter Paulsen

Authors
  1. Elke Rauscher-Gabernig
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  2. Robert Gabernig
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  3. Werner Brueller
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  5. Friedrich Bauer
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Correspondence to Elke Rauscher-Gabernig.

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Rauscher-Gabernig, E., Gabernig, R., Brueller, W. et al. Dietary exposure assessment of putrescine and cadaverine and derivation of tolerable levels in selected foods consumed in Austria. Eur Food Res Technol 235, 209–220 (2012). https://doi.org/10.1007/s00217-012-1748-1

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  • DOI: https://doi.org/10.1007/s00217-012-1748-1

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