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Determination of Antimicrobial Activity of Hesperidin Microemulsion Against Some Standard (ATCC) Gram Negative Bacteria

Yıl 2024, , 143 - 147, 02.12.2024
https://doi.org/10.32707/ercivet.1514585

Öz

Increasing antimicrobial resistance to synthetic antibiotics has attracted the interest of scientists in using naturally occurring compounds as effective antibacterial agents. It has been stated that hesperidin can also be effective against different pathogenic bacteria and can directly inhibit bacterial growth. This study aimed to determine the effecti-veness of Hesperidin against various ATCC strains (E. coli ATCC 25922, E. coli O157;H7 ATCC 43895, S. enteriditis NCTC, K. pneumonie ATCC 1705, A. hydrophila ATCC 7966). According to the MIC test results, the minimal ınhibitory concentration (MIC) values of E. coli, E. coli O157;H7, S. enteriditis and K. pneumonia bacteria for hesperidin were determined as 128 μg/mL, while the MIC value of A. hydrophila bacteria was determined as 64 μg/mL. In addition to these results, the MIC values for colistin for E. coli, K. pneumonia and A. hydrophila bacteria were determined as 0.5 μg/mL, while the MIC values for E. coli O157;H7 and S. enteriditis bacteria were 0.5 and 1 μg/mL, respectively. was determined as. These study results provide innovative evidence for hesperidin as a preventive and alternative antibac-terial treatment, especially in aquaculture.

Kaynakça

  • Abass EH, Zair SK, Mohammud TK, Nagem SA. Recovery of pure Hesperidin from Iraqi Sweet Oran-ges Peel and study the effect in some bacteria. Baghdad Sci J 2014; 11(2): 455-60.
  • Abuelsaad AS, Mohamed I, Allam G, Al-Solumani AA. Antimicrobial and immunomodulating activities of hesperidin and ellagic acid against diarrheic Ae-romonas hydrophila in a murine model. Life Sci 2013; 93(20); 714-22.
  • Antunes MS, Cattelan Souza L, Ladd FVL, Ladd AABL, Moreira AL, Bortolotto VC, Araújo SM, Prigol M, Nogueira CW, Boeira SP. Hesperidin ameliora-tes anxiety-depressive-like behavior in 6-OHDA model of Parkinson’s disease by regulating striatal cytokine and neurotrophic factors levels and dopa-minergic innervation loss in the striatum of mice. Mol Neurobiol 2020; 57: 3027-41.
  • Balakrishnan, K, Casimeer SC, Ghidan AY, Al Antary TM, Singaravelu A. Exploration of antioxidant, anti-bacterial activities of green synthesized hesperidin loaded PLGA nanoparticles. Biointerface Res Appl Chem 2021; 11(6): 14520-28.
  • Basile A, Sorbo S, Giordano S, Ricciardi L, Ferrara S, Montesano D, Castaldo CR, Vuotto ML, Ferrara L. Antibacterial and allelopathic activity of extract from Castanea sativa leaves. Fitoterapia 2000; 1: 110-6.
  • Bialvaei AZ, Samadi Kafil H. Colistin, mechanisms and prevalence of resistance. Current Med Res Opinion 2015; 31(4): 707-21.
  • Bouyahya A, Chamkhi I, Balahbib A, Rebezov M, Shariati MA, Wilairatana P, El Omari N. Mechanisms, anti-quorum-sensing actions, and clinical trials of medicinal plant bioactive compounds aga-inst bacteria: A comprehensive review. Molecules 2022; 27(5): 1484.
  • Chaieb K, Kouidhi B, Hosawi SB, Baothman OA, Zamzami MA, Altayeb HN. Computational screening of natural compounds as putative quorum sensing inhibitors targeting drug resistance bacte-ria: Molecular docking and molecular dynamics simulations. Comput Biol Medi 2022; 145: 105517.
  • Corciova A, Ciobanu C, Poiata A, Mircea C, Nicoles-cu A, Drobota M, Marangoci N. Antibacterial and antioxidant properties of hesperidin: β-cyclodextrin complexes obtained by different techniques. J Inc-lusion Phenom Macrocycl Chem 2015; 81: 71-84.
  • Esposito EP, Cervoni M, Bernardo M, Crivaro V, Cuc-curullo S, Imperi F, Zarrilli R. Molecular epidemiology and virulence profiles of colistin-resistant Kleb-siella pneumoniae blood isolates from the hospital agency “Ospedale dei Colli,” Naples, Italy. Front Microbiol 2018; 9: 1463.
  • Farhadi F, Khameneh B, Iranshahi M, Iranshahy M. Antibacterial activity of flavonoids and their structu-re-activity relationship: An update review. Phytother Res 2019; 33(1): 13-40.
  • Falagas, M. E., Kasiakou, S. K., Saravolatz, L. D. Colistin: the revival of polymyxins for the manage-ment of multidrug-resistant gram-negative bacterial infections. Clinic Infect Dis 2005; 40(9): 1333-41.
  • Fraga CG, Croft KD, Kennedy DO, Tomás-Barberán FA. The effects of polyphenols and other bioactives on human health. Food Funct 2019; 10(2): 514-28.
  • Gar A, Garg S, Zaneveld LJD, Singla AK. Chemistry and pharmacology of the citrus bioflavonoid hespe-ridin. Phytotherapy Res 2001; 15: 655-69.
  • González A, Casado J, Lanas Á. Fighting the antibio-tic crisis: Flavonoids as promising antibacterial drugs against Helicobacter pylori infection. Front Cell İnfect Microbi 2021; 11: 709749.
  • Guazelli CF, Fattori V, Ferraz CR, Borghi SM, Casag-rande R, Baracat MM, Verri Jr WA. Antioxidant and anti-inflammatory effects of hesperidin methyl chalcone in experimental ulcerative colitis. Chem Biol Interact 2021; 333: 109315.
  • Hindler JA, Humphries RM. Colistin MIC variability by method for contemporary clinical isolates of multidrug-resistant Gram-negative bacilli. J Clinic Micro-biol 2013; 51(6): 1678-84.
  • Hu Y, Li Y, Zhang W, Kou G, Zhou Z. Physical stability and antioxidant activity of citrus flavonoids in arabic gum-stabilized microcapsules: Modulation of whey protein concentrate. Food Hydrocoll 2018; 77: 588-97.
  • Ikram M, Muhammad T, Rehman SU, Khan A, Jo MG, Ali T, Kim MO. Hesperetin confers neuropro-tection by regulating Nrf2/TLR4/NF-κB signaling in an Aβ mouse model. Mol Neurobiol 2019; 56: 6293-309.
  • Kawaguchi K, Kikuchi S, Hasunuma R, Maruyama H, Yoshikawa T, Kumazawa YA citrus flavonoid hes-peridin suppresses infection-induced endotoxin shock in mice, Biol Pharm Bullet 2004; 27: 679-83.
  • Karayıldırım ÇK. Characterization and in vitro evolution of antibacterial efficacy of novel hesperidin microemulsion. Celal Bayar Univ J Sci 2017; 13(4): 943-7.
  • Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Shen J. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and hu-man beings in China: A microbiological and molecular biological study. Lancet infect Dis 2016; 16(2): 161-8.
  • Man MQ, Yang B, Elias PM. Benefits of hesperidin for cutaneous functions. J Evid Based Complementary Altern Med 2019: 2676307.
  • Matuschek E, Åhman J, Webster C, Kahlmeter G. Antimicrobial susceptibility testing of colistin-evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aerugi-nosa, and Acinetobacter spp. Clinic Microbiol Infect 2018; 24(8): 865-70.
  • Moon SH, Lee JH, Kim KT, Park YS, Nah SY, Ahn DU, Paik HD. Antimicrobial effect of 7-O-butylnaringenin, a novel flavonoid, and various natural flavonoids against Helicobacter pylori stra-ins. Int J Environ Res Public Health 2013; 10(11): 5459-69.
  • Morales AS, Fragoso de Araújo J, de Moura Gomes VT, Reis Costa AT, Prazeres Rodrigues DD, Porfi-da Ferreira TS, Rodrigues DP Ferreira TSP, De lima Filsner PHN, Felizardo MR, Micke Moreno A. Colistin resistance in Escherichia coli and Salmonella Enterica strains isolated from swine in Brazil. Sci World J 2012: 109795.
  • Muhammad T, Ikram M, Ullah R, Rehman SU, Kim MO. Hesperetin, a citrus flavonoid, attenuates LPS-induced neuroinflammation, apoptosis and memory impairments by modulating TLR4/NF-κB signaling. Nutrients 2019; 11(3): 648.
  • Musa AE, Omyan G, Esmaely F, Shabeeb D. Radioprotective effect of hesperidin: A systematic review. Medicina 2019; 55(7): 370.
  • National Committee for Clinical Laboratory Standards: Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, App-roved Standard-Eighth Edition, Wayne, Pennsylva-nia: NCCLS Document M7-A6, 2007.
  • Sader HS, Rhomberg PR, Flamm RK, Jones RN. Use of a surfactant (polysorbate 80) to improve MIC susceptibility testing results for polymyxin B and colistin. Diagn Microbiol Infect Dis 2012; 74(4): 412-4.
  • Suriyaprom S, Mosoni P, Leroy S, Kaewkod T, Des-vaux M, Tragoolpua Y. Antioxidants of fruit extracts as antimicrobial agents against pathogenic bacteria. Antioxidants 2022; 11(3): 602.
  • Tan TY, Ng SY. The in-vitro activity of colistin in Gram-negative bacteria. Singapore Med J 2006; 47(7); 621.
  • Truchado P, Gimenez-Bastida JA, Larrosa M, Castro-Ibáñez I, Espı́n JC, Tomas-Barberan FA, MT, Al-lende A. Inhibition of quorum sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. J Agric Food Chem 2012; 60(36): 8885-94.
  • Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, Malhotra-Kumar S. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Bel-gium, June 2016. Eurosurveillance 2016; 21(27): 30280.
  • Yamamoto M, Jokura H, Hashizume K, Oninami H, Shibuya Y, Suzuki A, Hase T, Shimotoyodome A. Hesperidin metabolite hesperetin-7-O-glucuronide, but not hesperetin-3'-O- glucuronide, exerts hypo-tensive, vasodilatory, and anti- inflammatory activity of extract from Castanea sativa leaves, Fitoterapia 2000; 71: 110-6.
  • Yi Z, Yu Y, Liang Y, Zeng B. In vitro antioxidant and antimicrobial activities of the extract of Pericarpium Citri Reticulatae of a new Citrus cultivar and its main flavonoids. LWT 2008; 41(4): 597-603.

Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti

Yıl 2024, , 143 - 147, 02.12.2024
https://doi.org/10.32707/ercivet.1514585

Öz

Sentetik antibiyotiklere karşı artan antimikrobiyal direnç, doğal olarak oluşan bileşiklerin etkili antibakteriyel ajanlar olarak kullanılması bilim insanlarının ilgisini çekmiştir. Doğal olarak oluşan bileşiklerden Hesperidin'in farklı patojen bakterilere karşı da etkili olabileceği, bakteriyel büyümeyi doğrudan engelleyebileceği belirtilmiştir. Bu çalışmada, Hes-peridin’in bazı ATCC suşlarına (Escherichia coli ATCC 25922, Escherichia coli O157;H7 ATCC 43895, Salmonella enteriditis NCTC, Klebsiella pneumonie ATCC 1705, Aeromonas hydrophila ATCC 7966) karşı etkinliğinin belirlenmesi amaçlanmıştır. Yapılan minimal inhibisyon konstrasyon (MİK) testi sonuçlarına göre Hesperidin için E. coli, E. coli O157;H7, S. enteriditis ve K. pneumonie bakterilerine ait MİK değerleri 128 μg/mL iken, A. hydrophila bakterisine ait MİK değeri 64 μg/mL olarak belirlenmiştir. Bu sonuçlara ek olarak, pozitif kontrol kolistin için E. coli, K. pneumonie ve A. hydrophila bakterilere ait MİK değerleri 0.5 μg/mL olarak belirlenirken, E. coli O157;H7 ve S. enteriditis bakterilerine ait MİK değerleri sırasıyla 0.5 ve 1 μg/mL olarak belirlenmiştir. Bu çalışma sonuçları Hesperidin’in özellikle su ürünleri yetiştiriciliğinde koruyucu ve alternatif bir antibakteriyel tedavi seçeneği olarak yenilikçi kanıtlar sunabilir.

Kaynakça

  • Abass EH, Zair SK, Mohammud TK, Nagem SA. Recovery of pure Hesperidin from Iraqi Sweet Oran-ges Peel and study the effect in some bacteria. Baghdad Sci J 2014; 11(2): 455-60.
  • Abuelsaad AS, Mohamed I, Allam G, Al-Solumani AA. Antimicrobial and immunomodulating activities of hesperidin and ellagic acid against diarrheic Ae-romonas hydrophila in a murine model. Life Sci 2013; 93(20); 714-22.
  • Antunes MS, Cattelan Souza L, Ladd FVL, Ladd AABL, Moreira AL, Bortolotto VC, Araújo SM, Prigol M, Nogueira CW, Boeira SP. Hesperidin ameliora-tes anxiety-depressive-like behavior in 6-OHDA model of Parkinson’s disease by regulating striatal cytokine and neurotrophic factors levels and dopa-minergic innervation loss in the striatum of mice. Mol Neurobiol 2020; 57: 3027-41.
  • Balakrishnan, K, Casimeer SC, Ghidan AY, Al Antary TM, Singaravelu A. Exploration of antioxidant, anti-bacterial activities of green synthesized hesperidin loaded PLGA nanoparticles. Biointerface Res Appl Chem 2021; 11(6): 14520-28.
  • Basile A, Sorbo S, Giordano S, Ricciardi L, Ferrara S, Montesano D, Castaldo CR, Vuotto ML, Ferrara L. Antibacterial and allelopathic activity of extract from Castanea sativa leaves. Fitoterapia 2000; 1: 110-6.
  • Bialvaei AZ, Samadi Kafil H. Colistin, mechanisms and prevalence of resistance. Current Med Res Opinion 2015; 31(4): 707-21.
  • Bouyahya A, Chamkhi I, Balahbib A, Rebezov M, Shariati MA, Wilairatana P, El Omari N. Mechanisms, anti-quorum-sensing actions, and clinical trials of medicinal plant bioactive compounds aga-inst bacteria: A comprehensive review. Molecules 2022; 27(5): 1484.
  • Chaieb K, Kouidhi B, Hosawi SB, Baothman OA, Zamzami MA, Altayeb HN. Computational screening of natural compounds as putative quorum sensing inhibitors targeting drug resistance bacte-ria: Molecular docking and molecular dynamics simulations. Comput Biol Medi 2022; 145: 105517.
  • Corciova A, Ciobanu C, Poiata A, Mircea C, Nicoles-cu A, Drobota M, Marangoci N. Antibacterial and antioxidant properties of hesperidin: β-cyclodextrin complexes obtained by different techniques. J Inc-lusion Phenom Macrocycl Chem 2015; 81: 71-84.
  • Esposito EP, Cervoni M, Bernardo M, Crivaro V, Cuc-curullo S, Imperi F, Zarrilli R. Molecular epidemiology and virulence profiles of colistin-resistant Kleb-siella pneumoniae blood isolates from the hospital agency “Ospedale dei Colli,” Naples, Italy. Front Microbiol 2018; 9: 1463.
  • Farhadi F, Khameneh B, Iranshahi M, Iranshahy M. Antibacterial activity of flavonoids and their structu-re-activity relationship: An update review. Phytother Res 2019; 33(1): 13-40.
  • Falagas, M. E., Kasiakou, S. K., Saravolatz, L. D. Colistin: the revival of polymyxins for the manage-ment of multidrug-resistant gram-negative bacterial infections. Clinic Infect Dis 2005; 40(9): 1333-41.
  • Fraga CG, Croft KD, Kennedy DO, Tomás-Barberán FA. The effects of polyphenols and other bioactives on human health. Food Funct 2019; 10(2): 514-28.
  • Gar A, Garg S, Zaneveld LJD, Singla AK. Chemistry and pharmacology of the citrus bioflavonoid hespe-ridin. Phytotherapy Res 2001; 15: 655-69.
  • González A, Casado J, Lanas Á. Fighting the antibio-tic crisis: Flavonoids as promising antibacterial drugs against Helicobacter pylori infection. Front Cell İnfect Microbi 2021; 11: 709749.
  • Guazelli CF, Fattori V, Ferraz CR, Borghi SM, Casag-rande R, Baracat MM, Verri Jr WA. Antioxidant and anti-inflammatory effects of hesperidin methyl chalcone in experimental ulcerative colitis. Chem Biol Interact 2021; 333: 109315.
  • Hindler JA, Humphries RM. Colistin MIC variability by method for contemporary clinical isolates of multidrug-resistant Gram-negative bacilli. J Clinic Micro-biol 2013; 51(6): 1678-84.
  • Hu Y, Li Y, Zhang W, Kou G, Zhou Z. Physical stability and antioxidant activity of citrus flavonoids in arabic gum-stabilized microcapsules: Modulation of whey protein concentrate. Food Hydrocoll 2018; 77: 588-97.
  • Ikram M, Muhammad T, Rehman SU, Khan A, Jo MG, Ali T, Kim MO. Hesperetin confers neuropro-tection by regulating Nrf2/TLR4/NF-κB signaling in an Aβ mouse model. Mol Neurobiol 2019; 56: 6293-309.
  • Kawaguchi K, Kikuchi S, Hasunuma R, Maruyama H, Yoshikawa T, Kumazawa YA citrus flavonoid hes-peridin suppresses infection-induced endotoxin shock in mice, Biol Pharm Bullet 2004; 27: 679-83.
  • Karayıldırım ÇK. Characterization and in vitro evolution of antibacterial efficacy of novel hesperidin microemulsion. Celal Bayar Univ J Sci 2017; 13(4): 943-7.
  • Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Shen J. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and hu-man beings in China: A microbiological and molecular biological study. Lancet infect Dis 2016; 16(2): 161-8.
  • Man MQ, Yang B, Elias PM. Benefits of hesperidin for cutaneous functions. J Evid Based Complementary Altern Med 2019: 2676307.
  • Matuschek E, Åhman J, Webster C, Kahlmeter G. Antimicrobial susceptibility testing of colistin-evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aerugi-nosa, and Acinetobacter spp. Clinic Microbiol Infect 2018; 24(8): 865-70.
  • Moon SH, Lee JH, Kim KT, Park YS, Nah SY, Ahn DU, Paik HD. Antimicrobial effect of 7-O-butylnaringenin, a novel flavonoid, and various natural flavonoids against Helicobacter pylori stra-ins. Int J Environ Res Public Health 2013; 10(11): 5459-69.
  • Morales AS, Fragoso de Araújo J, de Moura Gomes VT, Reis Costa AT, Prazeres Rodrigues DD, Porfi-da Ferreira TS, Rodrigues DP Ferreira TSP, De lima Filsner PHN, Felizardo MR, Micke Moreno A. Colistin resistance in Escherichia coli and Salmonella Enterica strains isolated from swine in Brazil. Sci World J 2012: 109795.
  • Muhammad T, Ikram M, Ullah R, Rehman SU, Kim MO. Hesperetin, a citrus flavonoid, attenuates LPS-induced neuroinflammation, apoptosis and memory impairments by modulating TLR4/NF-κB signaling. Nutrients 2019; 11(3): 648.
  • Musa AE, Omyan G, Esmaely F, Shabeeb D. Radioprotective effect of hesperidin: A systematic review. Medicina 2019; 55(7): 370.
  • National Committee for Clinical Laboratory Standards: Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, App-roved Standard-Eighth Edition, Wayne, Pennsylva-nia: NCCLS Document M7-A6, 2007.
  • Sader HS, Rhomberg PR, Flamm RK, Jones RN. Use of a surfactant (polysorbate 80) to improve MIC susceptibility testing results for polymyxin B and colistin. Diagn Microbiol Infect Dis 2012; 74(4): 412-4.
  • Suriyaprom S, Mosoni P, Leroy S, Kaewkod T, Des-vaux M, Tragoolpua Y. Antioxidants of fruit extracts as antimicrobial agents against pathogenic bacteria. Antioxidants 2022; 11(3): 602.
  • Tan TY, Ng SY. The in-vitro activity of colistin in Gram-negative bacteria. Singapore Med J 2006; 47(7); 621.
  • Truchado P, Gimenez-Bastida JA, Larrosa M, Castro-Ibáñez I, Espı́n JC, Tomas-Barberan FA, MT, Al-lende A. Inhibition of quorum sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. J Agric Food Chem 2012; 60(36): 8885-94.
  • Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, Malhotra-Kumar S. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Bel-gium, June 2016. Eurosurveillance 2016; 21(27): 30280.
  • Yamamoto M, Jokura H, Hashizume K, Oninami H, Shibuya Y, Suzuki A, Hase T, Shimotoyodome A. Hesperidin metabolite hesperetin-7-O-glucuronide, but not hesperetin-3'-O- glucuronide, exerts hypo-tensive, vasodilatory, and anti- inflammatory activity of extract from Castanea sativa leaves, Fitoterapia 2000; 71: 110-6.
  • Yi Z, Yu Y, Liang Y, Zeng B. In vitro antioxidant and antimicrobial activities of the extract of Pericarpium Citri Reticulatae of a new Citrus cultivar and its main flavonoids. LWT 2008; 41(4): 597-603.
Toplam 36 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Veteriner Gıda Hijyeni ve Teknolojisi
Bölüm Araştırma Makalesi
Yazarlar

Mukaddes Barel 0000-0002-1170-8632

Yayımlanma Tarihi 2 Aralık 2024
Gönderilme Tarihi 28 Kasım 2023
Kabul Tarihi 13 Şubat 2024
Yayımlandığı Sayı Yıl 2024

Kaynak Göster

APA Barel, M. (2024). Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 21(3), 143-147. https://doi.org/10.32707/ercivet.1514585
AMA Barel M. Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti. Erciyes Üniv Vet Fak Derg. Aralık 2024;21(3):143-147. doi:10.32707/ercivet.1514585
Chicago Barel, Mukaddes. “Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21, sy. 3 (Aralık 2024): 143-47. https://doi.org/10.32707/ercivet.1514585.
EndNote Barel M (01 Aralık 2024) Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21 3 143–147.
IEEE M. Barel, “Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti”, Erciyes Üniv Vet Fak Derg, c. 21, sy. 3, ss. 143–147, 2024, doi: 10.32707/ercivet.1514585.
ISNAD Barel, Mukaddes. “Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21/3 (Aralık 2024), 143-147. https://doi.org/10.32707/ercivet.1514585.
JAMA Barel M. Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti. Erciyes Üniv Vet Fak Derg. 2024;21:143–147.
MLA Barel, Mukaddes. “Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, c. 21, sy. 3, 2024, ss. 143-7, doi:10.32707/ercivet.1514585.
Vancouver Barel M. Hesperidin Mikroemülsiyonunun Bazı Standart (ATCC) Gram Negatif Bakterilere Karşı Antimikrobiyal Etkinliğinin Tespiti. Erciyes Üniv Vet Fak Derg. 2024;21(3):143-7.