Advertisement

The effect of smoking on the formation of biogenic amines in Circassian cheese

Research article
  • 205 Downloads

Abstract

In this study, the effect of smoking on the amount of biogenic amines (BA) in Circassian cheese was evaluated. The chemical and microbiological changes related to BA formation in smoked and non-smoked Circassian cheeses were evaluated after 0, 15, 30, 45, 60, and 90 days of storage. At each ending of storage time, tyramine (TYR) and histamine (HIS) could not be detected in any of the samples. Furthermore, tryptamine (TRYP) decreased significantly during storage. Also, cadaverine (CAD) in non-smoked cheese samples increased while CAD levels did not change significantly in smoked cheeses. A significant (p < 0.05) increase was observed in 2-phenylethylamine for both smoked and non-smoked Circassian cheeses while putrescine levels remained fairly the same. In conclusion, lower levels of total BA were detected in smoked samples, and smoking process improved the quality of Circassian cheeses.

Keywords

Smoked cheese Circassian cheese Biogenic amines Cheese quality 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

This study was funded by Sakarya University—Scientific Research Projects Unit, with the project number 2012-01-16-008.

References

  1. Ahmad JI (2003) Smoked foods, application of smoking. In: Benjamin C (ed) Encyclopedia of food sciences and nutrition, 2nd edn. Academic Press, Oxford, pp 5309–5316CrossRefGoogle Scholar
  2. Anlı RE, Vural N, Yılmaz S, Vural H (2004) The determination of biogenic amines in Turkish red wines. J Food Compos Anal 17:53–62CrossRefGoogle Scholar
  3. AOAC (2000) Acidity of cheese. Titrimetric method. AOAC 920.124. Official methods of analysis of AOAC International, 17th edn. Association of Analytical Chemists, Washington, DCGoogle Scholar
  4. Aydınol P (2010) The effect of smoke application methods on the characteristics of smoked Circassian cheese (Master’s thesis, Uludağ University, Bursa, Turkey). Retrieved from https://tez.yok.gov.tr/UlusalTezMerkezi/
  5. Benkerroum N (2016) Biogenic amines in dairy products: origin, incidence, and control means. Compr Rev Food Sci Food Saf 15:801–826CrossRefGoogle Scholar
  6. Bermúdez R, Franco D, Carballo J, Sentandreu MA, Lorenzo JM (2014) Influence of muscle type on the evolution of free amino acids and sarcoplasmic and myofibrillar proteins through the manufacturing process of Celta dry-cured ham. Food Res Int 56:226–235CrossRefGoogle Scholar
  7. Broadley KJ (2010) The vascular effects of trace amines and amphetamines. Pharmacol Ther 125:363–375CrossRefPubMedGoogle Scholar
  8. Budak HNF, Karahan AG, Çakmakçı ML (2008) Factors affecting histamine and tyramine formation in turkish white cheese. Hacet J Biol Chem 36:197–206Google Scholar
  9. El-Zahar KM, El-Zaher AMA, Ramadan MFJ (2014) Levels of biogenic amines in cheeses and their impact on biochemical and histological parameters in rats. Korean Soc Appl Biol Chem 57:73–81CrossRefGoogle Scholar
  10. Folkertsma B, Fox PF (1992) Use of Cd-ninhydrin reagent to assess proteolysis in cheese during ripening. J Dairy Res 59:217–224CrossRefGoogle Scholar
  11. Gardini F, Özogul Y, Suzzi G, Tabanelli G, Özogul F (2016) Technological factors affecting biogenic amine content in foods: a review. Front Microbiol 7:1218. doi: 10.3389/fmicb.2016.01218 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Halász A, Baráth Á, Simon-Sarkadi L, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Technol 5:42–49CrossRefGoogle Scholar
  13. IDF (2001) Milk. Determination of nitrogen content. Part 5: Determination of protein nitrogen content. Standard 020.5. International Dairy Federation. Brussels, BelgiumGoogle Scholar
  14. İlhan E (2012) The physical, chemical, biochemical, microbiological and sensory properties of smoked and unsmoked Circassian cheese. (Master’s thesis, Ondokuz Mayıs University, Samsun, Turkey). Retrieved from https://tez.yok.gov.tr/UlusalTezMerkezi/
  15. ISO (2004) Cheese and processed cheese—determination of the total solids content (Reference method). ISO 5534:2004 (IDF 4: 2004). International Standardization Organization, GenevaGoogle Scholar
  16. ISO (2006) Cheese and processed cheese—determination of chloride content, Potentiometric titration method. ISO 5943:2006 (IDF 88: 2006). International Standardization Organization, GenevaGoogle Scholar
  17. ISO (2008) Cheese, determination of fat content—Van Gulik method. ISO 3433:2008 (IDF 222: 2008). International Standardization Organization, GenevaGoogle Scholar
  18. Johnson ME, Kapoor R, McMahon DJ, McCoy DR, Narasimmon RG (2009) Reduction of sodium and fat levels in natural and processed cheeses: scientific and technological aspects. Compr Rev Food Sci Food Saf 8:252–268CrossRefGoogle Scholar
  19. Joosten HMLJ, Northolt MD (1987) Conditions allowing the formation of biogenic amines in cheese. 2. Decarboxylative properties of some non-starter bacteria. Neth Milk Dairy J 41:259–280Google Scholar
  20. Kalac P (2009) Recent advances in the research on biological roles of dietary polyamines in man. J Appl Biomech 7:65–74Google Scholar
  21. Linares DM, Martin MC, Ladero V, Alvarez MA, Fernandez M (2011) Biogenic amines in dairy products. Crit Rev Food Sci Nutr 51:691–703CrossRefPubMedGoogle Scholar
  22. Linares DM, Del Río B, Ladero V, Martínez N, Fernández M, Martín MC, Álvarez MA (2012) Factors influencing biogenic amines accumulation in dairy products. Front Microbiol 180:1–10Google Scholar
  23. Manca G, Porcu A, Ru A, Salaris M, Franco MA, De Santis EPL (2015) Comparison of γ-aminobutyric acid and biogenic amine content of different types of ewe’s milk cheese produced in Sardinia, Italy. Ital J Food Saf 4(4700):123–128Google Scholar
  24. McSweeney PLH, Sousa MJ (2000) Biochemical pathways for the production of flavor compounds in cheeses during ripening: a review. Lait 80:293–324CrossRefGoogle Scholar
  25. Naila A, Flint S, Fletcher G, Bremer P, Meerdink G (2010) Control of biogenic amines in food—existing and emerging approaches. J Food Sci 75:139–150CrossRefGoogle Scholar
  26. Novella-Rodríguez S, Veciana-Nogués MT, Trujillo-Mesa AJ, Vidal-Carou MC (2002) Profile of biogenic amines in goat cheese made from pasteurized and pressurized milks. J Food Sci 67:2940–2944CrossRefGoogle Scholar
  27. Nuñez M, García-Aser C, Rodríguez-Martin MA, Medina M, Gaya P (1986) The effect of ripening and cooking temperatures on proteolysis and lipolysis in Manchego cheese. Food Chem 21:115–123CrossRefGoogle Scholar
  28. Önal A (2007) A review: Current analytical methods for the determination of biogenic amines in foods. Food Chem 103:1475–1486CrossRefGoogle Scholar
  29. Öner Z, Karahan AG, Aloğlu H (2006) Changes in the microbiological and chemical characteristics of an artisanal Turkish white cheese during ripening. LWT Food Sci Technol 39:449–454CrossRefGoogle Scholar
  30. Pintado AI, Pinho O, Ferreira IM, Pintado MME, Gomes AM, Malcata FX (2008) Microbiological, biochemical and biogenic amine profiles of Terrincho cheese manufactured in several dairy farms. Int Dairy J 18:631–640CrossRefGoogle Scholar
  31. Pisano BM, Fadda EM, Deplano M, Corda A, Cosentino S (2006) Microbiological and chemical characterization of Fiore Sardo, a traditional Sardinian cheese made from ewe’s milk. Int J Dairy Technol 59:171–179CrossRefGoogle Scholar
  32. Santos SMH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231CrossRefGoogle Scholar
  33. Shalaby AR (1997) Significance of biogenic amines to food safety and human health. Food Res Int 29:675–690CrossRefGoogle Scholar
  34. Škaljac S, Petrović L, Tasić T, Ikonić P, Jokanović M, Tomović V et al (2014) Influence of smoking in traditional and industrial conditions on polycyclic aromatic hydrocarbons content in dry fermented sausages (Petrovská klobása) from Serbia. Food Control 40:12–18CrossRefGoogle Scholar
  35. Tapingkae W, Tanasupawat S, Parkin KL, Benjakul S, Visessanguan W (2010) Degradation of histamine by extremely halophilic archaea isolated from high salt-fermented fishery products. Enzyme Microb Technol 46:92–99CrossRefGoogle Scholar
  36. Torracca B, Nuvoloni R, Ducci M, Bacci C, Pedonese F (2015) Biogenic amines content of four types of “Pecorino” cheese manufactured in Tuscany. Int J Food Prop 18:999–1005CrossRefGoogle Scholar
  37. Üçüncüoğlu D (2009) Some properties of Circassian cheese which sold in Middle Blacksea region. (Master’s thesis, Ondokuz Mayıs University, Samsun, Turkey). Retrieved from https://tez.yok.gov.tr/UlusalTezMerkezi
  38. Upadhyay VK, McSweeney PLH, Magboul AAA, Fox PF (2004) Proteolysis in cheese during ripening. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP (eds) Cheese: chemistry, physics and microbiology. General aspects, vol 1, 3rd edn. Elsevier, Amsterdam, pp 392–433Google Scholar
  39. Uysal H, Kavas G, Kesenkas H, Akbulut N (2010) Some properties of traditional Circassian cheese produced in Turkey. Int J Dairy Sci 5:150–152CrossRefGoogle Scholar
  40. Vallejos JMM, Pham LJ, Barraquio VL (2012) Biogenic amines in some natural and processed cheeses sold in Laguna Province, Philippines. Philipp J Sci 141:111–115Google Scholar

Copyright information

© Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (BVL) 2017

Authors and Affiliations

  1. 1.Department of Food Engineering, Faculty of EngineeringSakarya UniversitySakaryaTurkey

Personalised recommendations