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Biberiye Esansiyel Yağı ve Nanoemülsiyonunun Balıkta Bozulma Etmeni Bakteriler ile Gıda Kaynaklı Patojenik Bakteriler Tarafından Üretilen Biyojenik Aminler Üzerine Etkilerinin incelenmesi

Year 2022, Volume: 32 Issue: 1, 199 - 212, 31.03.2022

Yılmaz Uçar Mustafa Durmuş Esmeray Küley Boğa Koray Korkmaz

https://doi.org/10.29133/yyutbd.1035443

Abstract

Biberiye esansiyel yağı (BEO) ve nanoemülsiyonunun (BNE) balıkta bozulma etmeni bakteriler (P. luteola, P. damselae, V. vulnificus, E. faecalis, S. liquefaciens ve P. mirabilis) ve gıda kaynaklı patojenik bakterilerin (S. Paratyphi A, S. aureus, K. pneumoniae ve E. faecalis) gelişimi ve biyojenik amin (BA) üretimleri üzerine etkileri tirozin dekarboksilaz sıvısında (TDB) HPLC yöntemi kullanılarak incelenmiştir. Ekstrakte edilmiş BEO uçucu bileşenleri GC-MS kullanılarak belirlenmiştir ve elde edilen BNE'nun fiziksel özellikleri (viskozite, termodinamik kararlılık, damlacık boyutu ve yüzey gerilimi) analiz edilmiştir. Tween 80, BEO ve BNE, patojen ve bozucu bakterilerin büyüme ve gelişme performanslarına inhibe edici yönde etkili olmuştur. Gruplar arasında amonyak (AMN) ve biyojenik amin (BA) üretiminde istatistiksel farklılıklar gözlenmiştir (p<0.05). En yüksek histamin (HIS) üretimi, bozucu E. feacalis (58.76 mg/L) suşunda ve en düşük V. vulnificus (2.29 mg/L) suşunda gözlenmiştir. Putresin (PUT), kadaverin (CAD), spermidin (SPD) ve 2-feniletilamin (PHEN) gibi hemen hemen tüm diğer BA'ler patojenler ve bozulma grupları tarafından üretilmiştir. S. aureus, en yüksek tiramin (TYR) üreten (143.05-702.88 mg/L) suş olmuştur. V. vulnificus tarafından HIS üretimi, BNE varlığında önemli ölçüde baskılanmıştır (p<0.05). Muamele gruplarının (Tween 80, BEO ve BNE) etkisi bakteri suşuna ve spesifik amine bağlı olarak değişse de, tüm muamele grupları genel olarak bakteriler tarafından AMN ve BA üretimini azaltmıştır. Sonuç olarak, mevcut çalışma test edilen tüm bakterilerin birden fazla amino asidi dekarboksile etme yeteneğine sahip olduğunu, biberiye esansiyel yağının nanoemülsiyona dönüştürülmüş formunun biyojen amin üretimlerini baskıladığını ve bunun işlenmiş veya paketlenmiş balık veya gıda ürünlerinde alternatif bir antimikrobiyal ajan olarak kullanılabileceğini göstermiştir.

Keywords

Nanoemülsiyon biberiye esansiyel yağı biyojenik amin bakteri tirozin dekarboksilaz sıvısı.

Supporting Institution

Ordu Üniversitesi, Bilimsel Araştırma Projeleri Birimi

Project Number

A-2012

References

  • Abdollahzadeh, E., Rezaei, M., & Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35(1), 177e183.
  • Al-zoreky, N. S., & Al–Taher, A. Y. (2015). Antibacterial activity of spathe from Phoenix dactylifera L. against some food-borne pathogens. Industrial Crops and Products, 65, 241-246.
  • Buňková, L., Buňka, F., Klčovská, P., Mrkvička, V., Doležalová, M., & Kráčmar, S. (2010). Formation of biogenic amines by Gram-negative bacteria isolated from poultry skin. Food Chemistry, 121(1), 203-206.
  • Chang, S. C., Kung, H. F., Chen, H. C., Lin, C. S., & Tsai, Y. H. (2008). Determination of histamine and bacterial isolation in swordfish fillets (Xiphias gladius) implicated in a food borne poisoning. Food Control, 19(1), 16-21.
  • Chang, Y., McLandsborough, L., & McClements, D. J. (2012). Physical properties and antimicrobial efficacy of thyme oil nanoemulsions: Influence of ripening inhibitors. Journal of Agricultural and Food Chemistry, 60(48), 12056-12063.
  • Chu, Y., Gao, C., Liu, X., Zhang, N., Xu, T., Feng, X., ... & Tang, X. (2020). Improvement of storage quality of strawberries by pullulan coatings incorporated with cinnamon essential oil nanoemulsion. LWT, 122, 109054.
  • Donsì, F., Cuomo, A., Marchese, E., & Ferrari, G. (2014). Infusion of essential oils for food stabilization: Unraveling the role of nanoemulsion-based delivery systems on mass transfer and antimicrobial activity. Innovative Food Science & Emerging Technologies, 22, 212-220.
  • Durlu-Özkaya, F., Ayhan, K., & Vural, N. (2001). Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Science, 58(2), 163-166.
  • Ghosh, V., Mukherjee, A., & Chandrasekaran, N. (2014). Eugenol-loaded antimicrobial nanoemulsion preserves fruit juice against, microbial spoilage. Colloids and Surfaces B: Biointerfaces, 114, 392-397.
  • Gokdogan, S., Özogul, Y., Kuley, E., Özogul, F., Kacar, C., & Ucar, Y. (2012). The influences of natural zeolite (cliptinolite) on ammonia and biogenic amine formation by foodborne pathogen. Journal of Food Science, 77(8), M452-M457.
  • Korkmaz, K., Tokur, B., & Uçar, Y. (2021). Enzimatik hidroliz yöntemi kullanılarak balık işleme atıklarından balık protein hidrolizatı üretimi. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 31(2), 502-513.
  • KučeroVá, K., SVobodoVá, H., Tůma, Š., Ondráčková, I., & Plockova, M. (2009). Production of biogenic amines by Enterococci. Czech Journal of Food Sciences, 2, 50-55.
  • Kuley, E., Balıkcı, E., Özoğul, İ., Gökdogan, S., & Özoğul, F. (2012). Stimulation of cadaverine production by foodborne pathogens in the presence of Lactobacillus, Lactococcus, and Streptococcus spp. Journal of Food Science, 77, 650- 658.
  • López-Sabater, E. I., Rodríguez-Jerez, J., Hernández-Herrero, M., & Mora-Ventura, M. T. (1996). Incidence of histamine-forming bacteria and histamine content in scombroid fish species from retail markets in the Barcelona area. International Journal of Food Microbiology, 28(3), 411-418.
  • Majeed, H., Antoniou, J., Shoemaker, C. F., & Fang, Z. (2015). Action mechanism of small and large molecule surfactant-based clove oil nanoemulsions against food-borne pathogens and real-time detection of their subpopulations. Archives of Microbiology, 197(1), 35-45.
  • McClements, D. J., & Rao, J. (2011). Food-grade nanoemulsions: Formulation, fabrication, properties, performance, biological fate, and potential toxicity. Critical Reviews in Food Science and Nutrition, 51(4), 285-330.
  • Niven Jr, C. F., Jeffrey, M. B., & Corlett Jr, D. A. (1981). Differential plating medium for quantitative detection of histamine-producing bacteria. Applied and Environmental Microbiology, 41(1), 321-322.
  • Nowak, A., Kalemba, D., Krala, L., Piotrowska, M., & Czyzowska, A. (2012). The effects of thyme (Thymus vulgaris) and rosemary (Rosmarinus officinalis) essential oils on Brochothrix thermosphacta and on the shelf life of beef packaged in high-oxygen modified atmosphere. Food Microbiology, 32, 212-6.
  • Özoğul, F. (2004). Production of biogenic amines by Morganella morganii, Klebsiella pneumoniae and Hafnia alvei using a rapid HPLC method. European Food Research and Technology, 219, 465–469.
  • Özogul, F., & Özogul, Y. (2007). The ability of biogenic amines and ammonia production by single bacterial cultures. European Food Research Technology, 225, 385–394.
  • Özogul, Y., Durmus, M., Ucar, Y., Özogul, F., & Regenstein, J. M. (2016). Comparative study of nanoemulsions based on commercial oils (sunflower, canola, corn, olive, soybean, and hazelnut oils): Effect on microbial, sensory, and chemical qualities of refrigerated farmed sea bass. Innovative Food Science & Emerging Technologies, 33, 422-430.
  • Özogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M., & Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT, 75, 677-684.
  • Özogul, Y., Boğa, E. K., Akyol, I., Durmus, M., Ucar, Y., Regenstein, J. M., & Köşker, A. R. (2020). Antimicrobial activity of thyme essential oil nanoemulsions on spoilage bacteria of fish and food-borne pathogens. Food Bioscience, 36, 100635.
  • Pereira, V., Dias, C., Vasconcelos, M., Rosa, E., & Saavedra, M. (2014). Antibacterial activity and synergistic effects between Eucalyptus globulus leaf residues (essential oils and extracts) and antibiotics against several isolates of respiratory tract infections (Pseudomonas aeruginosa). Industrial Crops and Products, 52, 1-7.
  • Redmond, J. W., & Tseng, A. (1979). High-pressure liquid chromatographic determination of putrescine, cadaverine, spermidine and spermine. Journal of Chromatography A, 170(2), 479-481.
  • Salvia-Trujillo, L., Rojas-Graü, A., Soliva-Fortuny, R., & Martín-Belloso, O. (2015). Physicochemical characterization and antimicrobial activity of food-grade emulsions and nanoemulsions incorporating essential oils. Food Hydrocolloids, 43, 547-556.
  • Seitter, M., Geng, B., & Hertel, C. (2011). Binding to extracellular matrix proteins and formation of biogenic amines by food-associated coagulase-negative Staphylococci. International Journal of Food Microbiology, 145, 483-7.
  • Shafiq, S., Shakeel, F., Talegaonkar, S., Ahmad, F. J., Khar, R. K., & Ali, M. (2007). Design and development of oral oil in water ramipril nanoemulsion formulation: in vitro and in vivo assessment. Journal of Biomedical Nanotechnology, 3(1), 28-44.
  • Telli, R., Gök, V., & Çağlar, A. (2006). Aromatik uçucu yağ bileşenlerinin gıdalardaki antibakteriyel etkileri. Türkiye 9. Gıda Kongresi; 24-26 Mayıs, Bolu 939.
  • ten Brink, B., Damink, C., Joosten, H. M. L. J., & In't Veld, J. H. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11(1), 73-84.
  • Uçar, Y. (2020a). Su ürünlerinde nisin uygulamaları. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 30(3), 639-651.
  • Uçar, Y. (2020b). Antioxidant effect of nanoemulsions based on citrus peel essential oils: Prevention of lipid oxidation in trout. European Journal of Lipid Science and Technology, 122(5), 1900405.
  • Yazgan, H., Ozogul, Y., & Kuley, E. (2019). Antimicrobial influence of nanoemulsified lemon essential oil and pure lemon essential oil on food-borne pathogens and fish spoilage bacteria. International Journal of Food Microbiology, 306, 108266.

Inhibitory Effect of Rosemary Essential Oil and Its Nanoemulsion on the Formation of Biogenic Amines by Food-Borne Pathogens and Fish Spoilage Bacteria

Year 2022, Volume: 32 Issue: 1, 199 - 212, 31.03.2022

Yılmaz Uçar Mustafa Durmuş Esmeray Küley Boğa Koray Korkmaz

https://doi.org/10.29133/yyutbd.1035443

Abstract

The effect of nanoemulsions based on rosemary essential oil (BNE) and its purified version (BEO) on the growth of fish spoilage bacteria (P. luteola, P. damselae, V. vulnificus, E. faecalis, S. liquefaciens, and P. mirabilis) and foodborne pathogens (S. Paratyphi A, S. aureus, K. pneumoniae, and E. faecalis) and their biogenic amine formation were investigated in tyrosine decarboxylase broth (TDB) using HPLC method. The flavour compounds of extracted BEO were determined using GC-MS. Physical properties of BNE (viscosity, thermodynamic stability, droplet size, and surface tension) were analysed. Tween 80, BEO, and BNE were inhibitory effects on the growth performances of the pathogenic and spoilage bacteria. Differences in ammonia (AMN) and biogenic amine (BA) production among groups were statistically significant (p<0.05). The highest HIS production was obtained by spoilage E. faecalis (58.76 mg L-1) and the lowest by V. vulnificus (2.29 mg L-1). Almost all other BAs such as PUT, CAD, SPD, and PHEN were formed by pathogens and spoilage groups. S. aureus (143.05-702.88 mg L-1) was the main high tyramine (TYR) producer in TDB. HIS production by V. vulnificus was considerably suppressed in the presence of BNE (p<0.05). Although the effect of treatment groups (Tween 80, BEO, and BNE) varied depending on the bacterial strain and specific amine, all groups generally decreased AMN and BA accumulation by bacteria. Consequently, the results show that all bacteria tested are capable of decarboxylating more than one amino acid and conversion of rosemary oil into nanoemulsion suppressed BA production activity and its nano-form can be used as an alternative antimicrobial agent in processed or packaged fish or food products.

Keywords

Bacteria Biogenic amine Essential oils Decarboxylase broth. Nanoemulsion

Project Number

A-2012

References

  • Abdollahzadeh, E., Rezaei, M., & Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35(1), 177e183.
  • Al-zoreky, N. S., & Al–Taher, A. Y. (2015). Antibacterial activity of spathe from Phoenix dactylifera L. against some food-borne pathogens. Industrial Crops and Products, 65, 241-246.
  • Buňková, L., Buňka, F., Klčovská, P., Mrkvička, V., Doležalová, M., & Kráčmar, S. (2010). Formation of biogenic amines by Gram-negative bacteria isolated from poultry skin. Food Chemistry, 121(1), 203-206.
  • Chang, S. C., Kung, H. F., Chen, H. C., Lin, C. S., & Tsai, Y. H. (2008). Determination of histamine and bacterial isolation in swordfish fillets (Xiphias gladius) implicated in a food borne poisoning. Food Control, 19(1), 16-21.
  • Chang, Y., McLandsborough, L., & McClements, D. J. (2012). Physical properties and antimicrobial efficacy of thyme oil nanoemulsions: Influence of ripening inhibitors. Journal of Agricultural and Food Chemistry, 60(48), 12056-12063.
  • Chu, Y., Gao, C., Liu, X., Zhang, N., Xu, T., Feng, X., ... & Tang, X. (2020). Improvement of storage quality of strawberries by pullulan coatings incorporated with cinnamon essential oil nanoemulsion. LWT, 122, 109054.
  • Donsì, F., Cuomo, A., Marchese, E., & Ferrari, G. (2014). Infusion of essential oils for food stabilization: Unraveling the role of nanoemulsion-based delivery systems on mass transfer and antimicrobial activity. Innovative Food Science & Emerging Technologies, 22, 212-220.
  • Durlu-Özkaya, F., Ayhan, K., & Vural, N. (2001). Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Science, 58(2), 163-166.
  • Ghosh, V., Mukherjee, A., & Chandrasekaran, N. (2014). Eugenol-loaded antimicrobial nanoemulsion preserves fruit juice against, microbial spoilage. Colloids and Surfaces B: Biointerfaces, 114, 392-397.
  • Gokdogan, S., Özogul, Y., Kuley, E., Özogul, F., Kacar, C., & Ucar, Y. (2012). The influences of natural zeolite (cliptinolite) on ammonia and biogenic amine formation by foodborne pathogen. Journal of Food Science, 77(8), M452-M457.
  • Korkmaz, K., Tokur, B., & Uçar, Y. (2021). Enzimatik hidroliz yöntemi kullanılarak balık işleme atıklarından balık protein hidrolizatı üretimi. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 31(2), 502-513.
  • KučeroVá, K., SVobodoVá, H., Tůma, Š., Ondráčková, I., & Plockova, M. (2009). Production of biogenic amines by Enterococci. Czech Journal of Food Sciences, 2, 50-55.
  • Kuley, E., Balıkcı, E., Özoğul, İ., Gökdogan, S., & Özoğul, F. (2012). Stimulation of cadaverine production by foodborne pathogens in the presence of Lactobacillus, Lactococcus, and Streptococcus spp. Journal of Food Science, 77, 650- 658.
  • López-Sabater, E. I., Rodríguez-Jerez, J., Hernández-Herrero, M., & Mora-Ventura, M. T. (1996). Incidence of histamine-forming bacteria and histamine content in scombroid fish species from retail markets in the Barcelona area. International Journal of Food Microbiology, 28(3), 411-418.
  • Majeed, H., Antoniou, J., Shoemaker, C. F., & Fang, Z. (2015). Action mechanism of small and large molecule surfactant-based clove oil nanoemulsions against food-borne pathogens and real-time detection of their subpopulations. Archives of Microbiology, 197(1), 35-45.
  • McClements, D. J., & Rao, J. (2011). Food-grade nanoemulsions: Formulation, fabrication, properties, performance, biological fate, and potential toxicity. Critical Reviews in Food Science and Nutrition, 51(4), 285-330.
  • Niven Jr, C. F., Jeffrey, M. B., & Corlett Jr, D. A. (1981). Differential plating medium for quantitative detection of histamine-producing bacteria. Applied and Environmental Microbiology, 41(1), 321-322.
  • Nowak, A., Kalemba, D., Krala, L., Piotrowska, M., & Czyzowska, A. (2012). The effects of thyme (Thymus vulgaris) and rosemary (Rosmarinus officinalis) essential oils on Brochothrix thermosphacta and on the shelf life of beef packaged in high-oxygen modified atmosphere. Food Microbiology, 32, 212-6.
  • Özoğul, F. (2004). Production of biogenic amines by Morganella morganii, Klebsiella pneumoniae and Hafnia alvei using a rapid HPLC method. European Food Research and Technology, 219, 465–469.
  • Özogul, F., & Özogul, Y. (2007). The ability of biogenic amines and ammonia production by single bacterial cultures. European Food Research Technology, 225, 385–394.
  • Özogul, Y., Durmus, M., Ucar, Y., Özogul, F., & Regenstein, J. M. (2016). Comparative study of nanoemulsions based on commercial oils (sunflower, canola, corn, olive, soybean, and hazelnut oils): Effect on microbial, sensory, and chemical qualities of refrigerated farmed sea bass. Innovative Food Science & Emerging Technologies, 33, 422-430.
  • Özogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M., & Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT, 75, 677-684.
  • Özogul, Y., Boğa, E. K., Akyol, I., Durmus, M., Ucar, Y., Regenstein, J. M., & Köşker, A. R. (2020). Antimicrobial activity of thyme essential oil nanoemulsions on spoilage bacteria of fish and food-borne pathogens. Food Bioscience, 36, 100635.
  • Pereira, V., Dias, C., Vasconcelos, M., Rosa, E., & Saavedra, M. (2014). Antibacterial activity and synergistic effects between Eucalyptus globulus leaf residues (essential oils and extracts) and antibiotics against several isolates of respiratory tract infections (Pseudomonas aeruginosa). Industrial Crops and Products, 52, 1-7.
  • Redmond, J. W., & Tseng, A. (1979). High-pressure liquid chromatographic determination of putrescine, cadaverine, spermidine and spermine. Journal of Chromatography A, 170(2), 479-481.
  • Salvia-Trujillo, L., Rojas-Graü, A., Soliva-Fortuny, R., & Martín-Belloso, O. (2015). Physicochemical characterization and antimicrobial activity of food-grade emulsions and nanoemulsions incorporating essential oils. Food Hydrocolloids, 43, 547-556.
  • Seitter, M., Geng, B., & Hertel, C. (2011). Binding to extracellular matrix proteins and formation of biogenic amines by food-associated coagulase-negative Staphylococci. International Journal of Food Microbiology, 145, 483-7.
  • Shafiq, S., Shakeel, F., Talegaonkar, S., Ahmad, F. J., Khar, R. K., & Ali, M. (2007). Design and development of oral oil in water ramipril nanoemulsion formulation: in vitro and in vivo assessment. Journal of Biomedical Nanotechnology, 3(1), 28-44.
  • Telli, R., Gök, V., & Çağlar, A. (2006). Aromatik uçucu yağ bileşenlerinin gıdalardaki antibakteriyel etkileri. Türkiye 9. Gıda Kongresi; 24-26 Mayıs, Bolu 939.
  • ten Brink, B., Damink, C., Joosten, H. M. L. J., & In't Veld, J. H. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11(1), 73-84.
  • Uçar, Y. (2020a). Su ürünlerinde nisin uygulamaları. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 30(3), 639-651.
  • Uçar, Y. (2020b). Antioxidant effect of nanoemulsions based on citrus peel essential oils: Prevention of lipid oxidation in trout. European Journal of Lipid Science and Technology, 122(5), 1900405.
  • Yazgan, H., Ozogul, Y., & Kuley, E. (2019). Antimicrobial influence of nanoemulsified lemon essential oil and pure lemon essential oil on food-borne pathogens and fish spoilage bacteria. International Journal of Food Microbiology, 306, 108266.
There are 33 citations in total.

Details

Primary Language English
Subjects Agricultural Engineering
Journal Section Articles
Authors

Yılmaz Uçar 0000-0002-6770-6652

Mustafa Durmuş 0000-0002-2836-5154

Esmeray Küley Boğa 0000-0002-0655-0105

Koray Korkmaz 0000-0003-2940-6592

Project Number A-2012
Publication Date March 31, 2022
Acceptance Date March 8, 2022
Published in Issue Year 2022 Volume: 32 Issue: 1

Cite

APA Uçar, Y., Durmuş, M., Boğa, E. K., Korkmaz, K. (2022). Inhibitory Effect of Rosemary Essential Oil and Its Nanoemulsion on the Formation of Biogenic Amines by Food-Borne Pathogens and Fish Spoilage Bacteria. Yuzuncu Yıl University Journal of Agricultural Sciences, 32(1), 199-212. https://doi.org/10.29133/yyutbd.1035443
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Yuzuncu Yil University Journal of Agricultural Sciences by Van Yuzuncu Yil University Faculty of Agriculture is licensed under a Creative Commons Attribution 4.0 International License.