Year 2019, Volume 3 , Issue 4, Pages 265 - 271 2019-12-24

Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens

Aykut BURĞUT [1]


The influences of aqueous and ethanolic extracts of propolis (1%) on growth of common Gram-negative (Salmonella Parathyphi A, Campylobacter jejuni, Yersinia enterocolitica and Klebsiella pneumoniae) and -positive (Listeria monocytogenes, Staphylococcus aureus and Enterococcus faecalis) food-borne pathogens and their biogenic amines (BAs) production were examined in tyrosine decarboxylase broth (TDB). The highest growth inhibitory activity was observed against Gram-negative S. Paratyphi A in the existence of ethanolic and aqueous  extracts of propolis, with 2.49 and 1.9 log reduction, respectively. Ethanolic extracts of propolis were more effective than that of aqueous  extract on growth inhibition of L. monocytogenes (p<0.05). Both extracts of propolis had significant effect on reducing ammonia production by bacteria (p<0.05). Tyramine, dopamine, agmatine and spermine were major amines formed in TDB. Tyramine production was the lowest with S. Paratyphi A (1.94 mg/L) and highest with E. faecalis (254.93 mg/L). The existence of ethanolic propolis extracts in TDB led to significantly fewer tyramine production by Gram-positive S. aureus, L. monocytogenes and E. faecalis, and Gram-negative C. jejuni (p<0.05). Histamine produced lower than 1.3 mg/L by all food-borne pathogens. Ethanolic extracts of propolis generally led to lower histamine production by bacteria. The influence of propolis on BAs production varied according to type of extracts, specific BAs and bacterial strains. However, the aqueous of propolis generally showed a synergistic effect on most of BAs mainly tyramine production by bacteria. Thus, the use of propolis ethanolic extracts appeared to be more suitable than aqueous extract to control tyramine production in foods.
Propolis, Tyramine, Food-borne pathogens, Food safety
  • Afrouzan, H., Tahghighi, A., Zakeri, S. and Es-haghi, A. (2018). Chemical Composition and Antimicrobial Activities of Iranian Propolis. Iranian Biomedical Journal, 22, 1, 50-65. doi: 10.22034/ibj.22.1.50.
  • Al-Ani, I., Zimmermann, S., Reichling, J. and Wink, M. (2018). Antimicrobial activities of European propolis collected from various geographic origins alone and in combination with antibiotics. Medicines, 5, 1, 2. doi: 10.3390/medicines5010002
  • Al Bulushi, I., Poole, S., Deeth, H.C., Dykes, G.A. (2009). Biogenic amines in fish: Roles in intoxication, spoilage, and nitrosamine formation. Critical Reviews in Food Science and Nutrition, 49, 369–377.
  • Apaydin, H. and Gümüş, T. (2018). Inhibitory effect of propolis (bee gum) against Staphylococcus aureus bacteria isolated from instant soups. Journal of Tekirdag Agricultural Faculty, 15, 1, 67-75.
  • Camino Feltes, M. M., Arisseto-Bragotto, A. P. and Block, J. M. (2017). Food quality, food-borne diseases, and food safety in the Brazilian food industry. Food Quality and Safety, 1, 1, 13-27. doi: 10.1093/fqsafe/fyx003.
  • Casquete, R., Castro, S. M., Jácome, S. and Teixeira, P. (2016). Antimicrobial activity of ethanolic extract of propolis in “Alheira”, a fermented meat sausage. Cogent Food and Agriculture, 2, 1, 1125773. doi: 10.1080/23311932.2015.1125774
  • Comas-Basté, O., Latorre-Moratalla, M. L., Sánchez-Pérez, S., Veciana-Nogués, M. T. and del Carmen Vidal-Carou, M. (2019). Histamine and other biogenic amines in food. From scombroid poisoning to histamine intolerance. In Biogenic Amines. IntechOpen. doi: 10.5772/intechopen.84333
  • Commission Regulation (EC) (2007). No: 1441/2007 Amending regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs. Official Journal of European Union L, 322, 12–29.
  • Connil, N., Breton, Y. L., Dousset, X., Auffray, Y., Rincé, A. and Préevost, H. (2002). Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Applied and Environtal Microbiology, 68, 3537–3544. doi: 10.1128/AEM.68.7.3537-3544.2002
  • Da Prada, M., Zurcher, G. and Wuthrich, I.(1988). On tyramine, food, beverages: the reversible MAO inhibitor monoclobemide. Journal of Neural Transmission, 26, 31–36.
  • De Figueiredo, S.M., Binda, N.S., Almeida, B.D.M., Lemos Abreu, S.R., de Abreu, J.A.S., Pastore G.M., Sato H.H., Toreti V.C., Tapia, E.V. and Park, Y.K. (2015). Green propolis: Thirteen constituents of polar extract and total flavonoids evaluated during six years through RP-HPLC. Current Drug Discovery Technologies, 12, 229–239.
  • De las Rivas, B., Marcobal, A., Carrascosa, A. and Munoz, R. (2006). PCR detection offood bacteria producing the biogenic amines histamine, tyramine, putrescineand cadaverine. Journal of Food Protection, 69, 2509–2514. doi: 10.4315/0362-028X-69.10.2509
  • De Palencia, P. F., Fernández, M., Mohedano, M. L., Ladero, V., Quevedo, C., Alvarez, M. A. and López, P. (2011). Role of tyramine synthesis by food-borne Enterococcus durans in adaptation to the gastrointestinal tract environment. Applied and Environmental Microbiology, 77, 2, 699-702. doi: 10.1128/AEM.01411-10
  • Fernández, M., Linares, D. M., del Río, B., Ladero, V. and Alvarez, M. A. (2007). HPLC quantification of biogenic amines in cheeses: correlation with PCR-detection of tyramine-producing microorganisms. Journal of Dairy Research, 74,3, 276-282. doi: 10.1017/S0022029907002488
  • Gram, L. and Dalgaard, P. (2002). Fish spoilage bacteria-problems and solutions. Current Opinion in Biotechnology, 13, 262–266. doi: 10.1016/S0958-1669(02)00309-9
  • Hazem, A., Popescu, C.V., Crisan, J., Popa, M., Chifiriuc, M., Pircalabioru, G.G. and Lupuliasa, D. (2017). Antibacterial efficiency of five propolis extracts on planktonic and adherent microbial strains. Farmacia, 65, 5, 813-818.
  • Karovičová, J. and Kohajdová, Z. (2005). Biogenic amines in food. Chemical Papers, 59, 1, 70-79.
  • Kim, Y. H. and Chung, H. J. (2011). The effects of Korean propolis against foodborne pathogens and transmission electron microscopic examination. New Biotechnology, 28, 6, 713-718. doi: 10.1016/j.nbt.2010.12.006
  • Klausen, N.K. and Huss, H.H. (1987). A rapid method for detection of histamine-producing bacteria. International Journal of Food Microbiology, 5, 137-146.
  • Kubiliene, L., Laugaliene, V., Pavilonis, A., Maruska, A., Majiene, D., Barcauskaite, K. and Savickas, A. (2015). Alternative preparation of propolis extracts: comparison of their composition and biological activities. BMC Complementary and Alternative Medicine, 15, 156, 1-7. doi: 10.1186/s12906-015-0677-5
  • Kuley, E. and Özogul, F. (2011). Synergistic and antagonistic effect of lactic acid bacteria on tyramine production by food-borne pathogenic bacteria in tyrosine decarboxylase broth. Food Chemistry, 127, 3, 1163-1168. doi: 10.1016/j.foodchem.2011.01.118
  • 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. Frontiers in Microbiology, 9, 1015, 1-9. doi: 10.3389/fmicb.2018.01015
  • Liu, Y., Cao, Y., Wang, T., Dong, Q., Li, J. and Niu, C. (2019). Detection of 12 common food-borne bacterial pathogens by TaqMan real-time PCR using a single set of reaction conditions. Frontiers in Microbiology, 10, 222, 1-9. doi: 10.3389/fmicb.2019.00222
  • Lorenzo, J. M., Martínez, S., Franco, I. and Carballo, J. (2007). Biogenic amine content during the manufacture of dry-cured lacón, a Spanish traditional meat product: Effect of some additives. Meat Science, 77, 2, 287-293. doi: 10.1016/j.meatsci.2007.03.020
  • Lu, L. C., Chen, Y. W. and Chou, C. C. (2005). Antibacterial activity of propolis against Staphylococcus aureus. International Journal of Food Microbiology, 102, 2, 213-220. doi: 10.1016/j.ijfoodmicro.2004.12.017
  • Maintz, L. and Novak, N. (2007). Histamine and histamine intolerance. The American Journal of Clinical Nutrition 85, 1185–1196. doi: 10.1093/ajcn/85.5.1185
  • Majiene, D., Trumbeckaite, S., Pavilonis, A., Savickas, A. and Martirosyan, D. M. (2007). Antifungal and antibacterial activity of propolis. Current Nutrition and Food Science, 3, 4, 304-308.
  • Marcobal, A., De Las Rivas, B., Landete, J. M., Tabera, L. and Muñoz, R. (2012). Tyramine and phenylethylamine biosynthesis by food bacteria. Critical Reviews in Food Science and Nutrition,52, 5, 448-467. doi: 10.1080/10408398.2010.500545
  • Nedji, N. and Loucif-Ayad, W. (2014). Antimicrobial activity of Algerian propolis in foodborne pathogens and its quantitative chemical composition. Asian Pacific Journal of Tropical Disease, 4, 6, 433-437. doi: 10.1016/S2222-1808(14)60601-0
  • Özogul, F. and Özogul, Y. (2007). The ability of biogenic amines and ammonia production by single bacterial cultures. European Food Research and Technology, 225, 385–394. doi: 10.1007/s00217-006-0429-3
  • Özogul, F., Kaçar, Ç. and Kuley, E. (2015). The impact of carvacrol on ammonia and biogenic amine production by common foodborne pathogens. Journal of Food Science, 80, 12, M2899-M2903. doi: 10.1111/1750-3841.13140
  • Pobiega, K., Kraśniewska, K., Przybył, J. L., Bączek, K., Żubernik, J., Witrowa-Rajchert, D. and Gniewosz, M. (2019). Growth biocontrol of foodborne pathogens and spoilage microorganisms of food by polish propolis extracts. Molecules, 24, 16, 2965. doi: 10.3390/molecules24162965
  • Przybyłek, I. and Karpiński, T. M. (2019). Antibacterial properties of propolis. Molecules, 24, 11, 1-17. doi: 10.3390/molecules24112047
  • Satoshi, M., Yoshikazu, I., Yukio, N., Shozo, O., Takashi, S., Yoko, A. and Yoshinori, N. (2005). Identification of caffeoylquinic acid derivatives from Brazilian propolis as constituents involved in induction of granulocytic differentiation of HL-60 cells. Bioorganic and Medicinal Chemistry, 13, 5814–5818. doi: 10.1016/j.bmc.2005.05.044
  • Silla-Santos, M. H. (1996). Biogenic amines: their importance in foods. International Journal of Food Microbiology, 29, 2-3, 213-31. doi: 10.1016/0168-1605(95)00032-1
  • Sforcin J.M. and Bankova V. (2011). Propolis: Is there a potential for the development of new drugs? Journal of Ethnopharmacology, 133, 253–260. doi: 10.1016/j.jep.2010.10.032
  • Shalaby, A.R. (1996). Significance of biogenic amines to food safety and human health. Food Research International, 29, 7, 675-690. doi: 10.1016/S0963-9969(96)00066-X
  • Temiz, A., Şener, A., Tüylü, A. Ö., Sorkun, K. and Salih, B. (2011). Antibacterial activity of bee propolis samples from different geographical regions of Turkey against two foodborne pathogens, Salmonella enteritidis and Listeria monocytogenes. Turkish Journal of Biology, 35, 4, 503-511. doi: 10.3906/biy-0908-22
  • Wendakoon, C.N. and Sakaguchi, M. (1995). Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. Journal of Food Protection, 58, 3, 280-283. doi: 10.4315/0362-028X-58.3.280
Primary Language en
Subjects Agriculture, Agricultural, Engineering, Agriculture, Multidisciplinary, Agriculture, Dairy and Animal Science
Published Date December 2019
Journal Section Research Articles
Authors

Orcid: 0000-0002-5335-5070
Author: Aykut BURĞUT (Primary Author)
Institution: CUKUROVA UNIVERSITY, FACULTY OF AGRICULTURE
Country: Turkey


Dates

Application Date : September 1, 2019
Acceptance Date : December 17, 2019
Publication Date : December 24, 2019

Bibtex @research article { jaefs641253, journal = {International Journal of Agriculture Environment and Food Sciences}, issn = {}, eissn = {2618-5946}, address = {Dicle University Faculty of Agriculture Department of Horticulture, 21280 Diyarbakir / Turkey}, publisher = {Gültekin ÖZDEMİR}, year = {2019}, volume = {3}, pages = {265 - 271}, doi = {10.31015/jaefs.2019.4.11}, title = {Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens}, key = {cite}, author = {BURĞUT, Aykut} }
APA BURĞUT, A . (2019). Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens. International Journal of Agriculture Environment and Food Sciences , 3 (4) , 265-271 . DOI: 10.31015/jaefs.2019.4.11
MLA BURĞUT, A . "Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens". International Journal of Agriculture Environment and Food Sciences 3 (2019 ): 265-271 <https://dergipark.org.tr/en/pub/jaefs/issue/50908/641253>
Chicago BURĞUT, A . "Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens". International Journal of Agriculture Environment and Food Sciences 3 (2019 ): 265-271
RIS TY - JOUR T1 - Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens AU - Aykut BURĞUT Y1 - 2019 PY - 2019 N1 - doi: 10.31015/jaefs.2019.4.11 DO - 10.31015/jaefs.2019.4.11 T2 - International Journal of Agriculture Environment and Food Sciences JF - Journal JO - JOR SP - 265 EP - 271 VL - 3 IS - 4 SN - -2618-5946 M3 - doi: 10.31015/jaefs.2019.4.11 UR - https://doi.org/10.31015/jaefs.2019.4.11 Y2 - 2019 ER -
EndNote %0 International Journal of Agriculture Environment and Food Sciences Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens %A Aykut BURĞUT %T Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens %D 2019 %J International Journal of Agriculture Environment and Food Sciences %P -2618-5946 %V 3 %N 4 %R doi: 10.31015/jaefs.2019.4.11 %U 10.31015/jaefs.2019.4.11
ISNAD BURĞUT, Aykut . "Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens". International Journal of Agriculture Environment and Food Sciences 3 / 4 (December 2019): 265-271 . https://doi.org/10.31015/jaefs.2019.4.11
AMA BURĞUT A . Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens. int. j. agric. environ. food sci.. 2019; 3(4): 265-271.
Vancouver BURĞUT A . Aqueous and ethanolic extracts of propolis for the control of tyramine production by food-borne pathogens. International Journal of Agriculture Environment and Food Sciences. 2019; 3(4): 271-265.