Araştırma Makalesi
BibTex RIS Kaynak Göster

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

Yıl 2019, Cilt: 3 Sayı: 4, 265 - 271, 24.12.2019
https://doi.org/10.31015/jaefs.2019.4.11

Öz

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 e
xistence 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
.










Kaynakça

  • 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
Yıl 2019, Cilt: 3 Sayı: 4, 265 - 271, 24.12.2019
https://doi.org/10.31015/jaefs.2019.4.11

Öz

Kaynakça

  • 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
Toplam 39 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Ziraat Mühendisliği, Ziraat Mühendisliği (Diğer), Ziraat, Veterinerlik ve Gıda Bilimleri, Hayvansal Üretim (Diğer)
Bölüm Makaleler
Yazarlar

Aykut Burğut 0000-0002-5335-5070

Yayımlanma Tarihi 24 Aralık 2019
Gönderilme Tarihi 1 Eylül 2019
Kabul Tarihi 17 Aralık 2019
Yayımlandığı Sayı Yıl 2019 Cilt: 3 Sayı: 4

Kaynak Göster

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. https://doi.org/10.31015/jaefs.2019.4.11

by-nc.png

International Journal of Agriculture, Environment and Food Sciences dergisinin içeriği, Creative Commons Alıntı-GayriTicari (CC BY-NC) 4.0 Uluslararası Lisansı ile yayınlanmaktadır. Söz konusu telif, üçüncü tarafların içeriği uygun şekilde atıf vermek koşuluyla, ticari olmayan amaçlarla paylaşımına ve uyarlamasına izin vermektedir. Yazarlar, International Journal of Agriculture, Environment and Food Sciences dergisinde yayınlanmış çalışmalarının telif hakkını elinde tutar. 

Web: dergipark.org.tr/jaefs  E-mail: editor@jaefs.com WhatsApp: +90 850 309 59 27