Evaluation of Antibacterial Effect of Honey on ESBL and Biofilm-Producing Enterobacterales

Seda Özdikmenli Tepeli; Burcu Kaya; Dilvin İpek

doi:10.18016/ksutarimdoga.vi.971261

TR EN

Balın GSBL ve Biyofilm Üreten Enterobacterales Üzerindeki Antibakteriyel Etkisinin Değerlendirilmesi

Öz

Mastitis, süt veriminin düşmesine ve ekonomik kayıplara neden olan bir meme bezi hastalığıdır. Mastitis bakteriyolojiktir; bu nedenle tedavilerinde genellikle antibiyotikler kullanılır. Mastitis tedavisinde antibiyotik kullanımının azaltılması için arı ürünleri, fitoterapi, uçucu yağlar gibi alternatif doğal tedavi yöntemleri değerlendirilmektedir. Bu çalışmada, distile su ve borik asit (%2) solventlerinde çözündürülen çiçek ve meşe balı örneklerinin ESBL ve biyofilm üreticisi Enterobacterales patojenleri üzerindeki in vitro antibakteriyel etkisi araştırıldı. Amaç bal/borik asit solüsyonunun büyükbaş göğüs yüzeylerinde doğal bir antiseptik solüsyon olarak mastitise karşı kullanılabilirliğini ortaya koymaktır. Borik asit ve distile su çözücülü bal çözeltileri arasında istatistiksel olarak anlamlı bir fark yoktur. Çiçek balı çözeltilerinde artan bal oranına göre antibakteriyel etkiler artmıştır. Ancak borik asit çözeltisinde çözülen meşe balının antibakteriyel etkinliği distile suda çözünenden daha yüksekti. Çiçek ve meşe balı örnekleri arasındaki istatistiksel ilişki analizi sonucunda çiçek balı örneklerinin antibakteriyel etkileri meşe balı örneklerine göre daha yüksek bulunmuştur (p<0.05) (R=0,825). Bu çalışma ile literatürde ilk defa bal ve borik asit ile mastitis tedavisine alternatif bir formülasyon geliştirilmiştir.

Anahtar Kelimeler

Evaluation of Antibacterial Effect of Honey on ESBL and Biofilm-Producing Enterobacterales

Abstract

Mastitis is a mammary gland inflammatory disease that causes milk yield reduction and economic losses. Mastitis is bacteriological and antibiotics are usually used for treatment. Alternative natural treatment methods such as bee products, phytotherapy, and essential oils were evaluated to reduce the use of antibiotics in the treatment of mastitis. In this study, the in vitro antibacterial effect of flower and oak honey samples dissolved in distilled water and boric acid (2%) on ESBL and biofilm-producing Enterobacterales pathogens was investigated. The aim was to establish the usability of honey/boric acid solution against mastitis as a natural antiseptic solution for bovine udder surfaces. Honey samples were studied by dissolving in distilled water and boric acid (2%) solvents. There was no significant statistical difference between honey solutions using distilled water and boric acid (p>0.05). Antibacterial effects were increased according to the increasing honey proportion in flower honey solutions. However, the antibacterial activity of oak honey dissolved in boric acid solution was higher than dissolved in distilled water. As a result of the statistical correlation analysis between flower and oak honey samples, antibacterial effects of flower honey samples were determined to be higher than oak honey samples (p<0.05) (R=0.825). An alternative formulation for mastitis treatment with honey and boric acid was developed for the first time in the literature.

Keywords

Teşekkür

We are thankful to Assoc. Prof. Dr. Nükhet N. Demirel Zorba and her laboratory members for their kind support about standard bacterial strains, Food Engineering Department, Çanakkale Onsekiz Mart University, Çanakkale, Turkey. This research received no grant from any funding agency/sector.

Kaynakça

Abdalhamed A M, Zeedan G S G, Abou Zeina H A A 2018. Isolation and identification of bacteria causing mastitis in small ruminants and their susceptibility to antibiotics, honey, essential oils, and plant extracts. Vet World 11(3): 355–362.
Al-Masaudi S B, Hussain M B, Al-Maaqar S M, Al Jaouni S, Harakeh S 2021. Corrigendum to “In vitro antibacterial activity of honey against multidrug-resistant Shigella sonnei” Compl Ther Clin Pract 43: 101283.
Anonymous 2006. T.C. Erciyes Üniversitesi Sağlik Uygulama ve Araştirma Merkezi Eczanede Yapilan Majistraller. https://hastaneler.erciyes. edu.tr /Files/ formused/8d0300d8-55d9-45be-8dde-21e8efdd805f. pdf (Retrieved date: 20.10.2021).
Anonymous 2019. Majistral Rehberi. https://www. aeo.org.tr/Files/Yayinlar/majistral-kitapcik -revize-web.pdf (Retrieved date: 20.10. 2021).
Anonymous 2021a. file:///C:/Users/burcu/Downloads/ Ar%C4%B1c%C4%B1l%C4%B1k%20%C3%9Cr%C3%BCn%20Raporu%202021-320%20TEPGE.pdf (Retrieved date:20.11.2021).
Anonymous 2021b. https://www.ncbi.nlm.nih.gov/ (Retrieved date:20.11.2021).
Bacayo M F D C, Shafi S F, Choon W C, Fattepur S, Nilugal K C, Khan J, Asmani F, Yusuf E 2018. A comparative study of the antimicrobial activity of wild (Tualang) honey and artificial honey against methecillin- resistant Staphylococcus aureus, Streptococcus pneumoniae and Klebsiella pneumoniae. Proceedings of BROMO Conference.
Bal Y 2011. Organik süt ineği işletmelerinde mastitis sorununa yaklaşımlar. Vet Hekim Der Derg 82: 7-14

Baltrušaitytė V, Venskutonis P R, Čeksterytė V 2007. Radical scavenging activity of different floral origin honey and beebread phenolic extracts. Food Chem 101(2): 502–514.
Baykam N 2007. Wound care: antimicrobial treatment of the wound. Hastane Enfek Derg11: 27-32.
Boorn K L, Khor Y Y, Sweetman E, Tan F, Heard T A, Hammer K A 2010. Antimicrobial activity of honey from the stingless bee Trigona carbonaria determined by agar diffusion, agar dilution, broth microdilution and time-kill methodology. J Appl Microbiol 108(5): 1534–1543.
Čabarkapa I, Škrinjar M, Levic J 2015. Biofilm forming ability of Salmonella enteritidis in vitro. Acta Vet Belgrade 65: 371-389.
Çakır Y, Çobanoğlu D N, Dervişoğlu G, Koçyiğit S, Karahan D, Yelkovan S 2020. Determination antimicrobial activity, palynological characteristics and chemical composition of some honey samples from Turkey. Mellifera 20(1): 41-60.
Cengiz S, Dinç G, Söğüt MÜ 2014. Detection of several virulence properties, antibiotic resistance and phylogenetic relationship in E. coli isolates originated from cow mastitis. Acta Vet 64.
Çil G İ, Küplülü Ö, Cengiz G, Korkmaz S D, Arslan B, Gürcan S 2020. Antibacterial activity of Turkish honey against selected foodborne pathogens. Ankara Üni Vet Fak Derg 67:413–418.
Cinar A 2020. Determination of Antimicrobial Activities of Different Flower Honeys. U.Bee.J. 20(1): 38-50.
Dahmen S, Métayer V, Gay E, Madec J Y, Haenni M 2013. Characterization of extended-spectrum beta-lactamase (ESBL)-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet Microbiolo 162 (2-4): 793-799.
Das A, Guha C, Biswas U, Jana P S, Chatterjee A, Samanta I 2017. Detection of emerging antibiotic resistance in bacteria isolated from subclinical mastitis in cattle in West Bengal. Vet World 10(5): 517–520.
Demircan B, Velioğlu Y S 2020. Gıda ve çevreden alınan bor bileşiklerinin toksikolojik değerlendirmesi. Akademik Gıda 18(3):312-322.
Deniz D, Selvi S 2021. Kazdağı Milli Parkı’nın (Edremit/Balıkesir) çalı ve ağaç florası. AKU-FEMÜBİD 21(5): 1005-1015.
EFSA Panel on Biological Hazards 2011. Scientific opinion on the public health risks of bacterial strains producing extended-spectrum β-lactamases and/or AmpC β-lactamases in food and food-producing animals 9:2322.
Erturk O, Sahin H, Kolayli S, Col Ayvaz M 2014. Antioxidant and antimicrobial activity of East Black Sea Region honeys. Turkish J Biochem 39(1): 99–106.
EUCAST 2013. European committee on antimicrobial susceptibility testing guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. The European Committee on Antimicrobial Susceptibility Testing, Basel, Switzerland.
Güneş M E, Şahin S, Demir C, Borum E, Tosunoğlu A 2016. Determination of phenolic compounds profile in chestnut and floral honeys and their antioxidant and antimicrobial activities. J Food Biochem 41(3): e12345.
Hui Y, Yuan X D, Zhang T 2016. Vaginal retained boric acid preparation and preparation method there of China, CN105362289B.
Ibrahim D R, Dodd C E, Stekel D J, Ramsden S J, Hobman J L 2016. Multidrug resistant, extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiol Ecol 92(4). fiw013
İlhan Z, Ekin İ H, Gülaydın Ö 2019. Antimicrobial activity of boric acid solution against Listeria monocytogenes and Staphylococcus aureus. Van Vet J 30: 163-166.
İpek D 2017. Applicability of Ezine Cheese process lines disinfection by new disinfectant formulas antibiofilm-antiquorum sensing agents. Çanakkale Onsekiz Mart University Graduate School of Natural and Applied Sciences, Department of Food Engineering, PhD Thesis, p .166.
İpek D, Zorba NN 2018. Importance of biofilms on dairy industry safety understanding microbial pathogens (Current knowledge and educational ideas on antimicrobial research, Formatex Research Center, Spain: Ed. Torres-Hergueta E, Méndez-Vilas A) 146-152.
Kolayli S, Sahin H, Can Z, Yildiz O, Sahin K 2016. Honey shows potent inhibitory activity against the bovine testes hyaluronidase. J Enzyme Inhib Med Chem 31(4): 599–602.
Krömker V N, Wente N, Zhang Y, Bolte J, Renner R, Schmenger A, Titze I, Wallis J, Mayer P, Klocke D 2019. Comparison of a non-antibiotic treatment with an antibiotic treatment of chronic mastitis. Milchwissenschaft 72: 34-38.
Kwakman P H S, Van den Akker J P C, Güçlü A, Aslami H, Binnekade J M, de Boer L, Boszhard L, Paulus F,
Middelhoek P, te Velde A A, Vandenbroucke‐Grauls C M J E, Schultz M J, Zaat S A J 2008. Medical‐Grade honey kills antibiotic‐resistant bacteria ın vitro and eradicates skin colonization. Clin Infec Dis 46(11): 1677–1682.
Laranjo M, Andrade N, Queiroga C 2018. Antibiofilm activity of propolis extracts. Understanding microbial pathogens: current knowledge and educational ideas on antimicrobial research. (Current knowledge and educational ideas on antimicrobial research, Formatex Research Center, Spain: Ed. Torres-Hergueta E, Méndez-Vilas A) 1-8.
Leitner G, Zilberman D, Papirov E, Shefy S 2018. Assessment of acoustic pulse therapy (APT), a non-antibiotic treatment for dairy cows with clinical and subclinical mastitis. Plos One 13(7): e0199195.
Liu Q, Liu Z, Zhang C, Xu Y, Li X, Gao H 2021. Effects of 3% boric acid solution on cutaneous Candida albicans infection and microecological flora mice. Front Microbiol 12: 709880.
Magesh H, Kumar A, Alam A, Sekar U 2013. Identification of natural compounds which inhibit biofilm formation in clinical isolates of Klebsiella pneumoniae. Indian J Exp Biol 51: 764-772.
Mercan N, Guvensen A, Celik A, Katircioglu H 2007. Antimicrobial activity and pollen composition of honey samples collected from different provinces in Turkey. Nat Prod Res 21(3): 187–195.
Milanov D, Prunić B, Velhner M, Todorović D, Polaček V 2015. Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains ısolated from milk of cows with mastitis. Acta Vet 65(2): 202–216.
Nadia Z, Kheira G 2018. Impact of milking modalities on the occurrence of subclinical mastitis and the anti-bacterial effect of honey on isolated bacteria (Escherichia coli) South Asian J Exp Bio 8(1), 13-18.
Ni̇sbet C, Aker D 2020. Antioxidant activities, total phenolic and flavonoid contents of honey collected from different botanical origins. Ankara Üniv Vet Fak Derg 67: 133–136.
Nolan V C, Harrison J, Cox JAG 2019. Dissecting the antimicrobial composition of honey. Antibiotics 8(4): 251.
Ögedey E D, Cömert F, Köktürk F, Külah C, Aktaş E 2016. Detection of CTX-M Enzymes in ESBL (Extended-Spectrum Beta-Lactamases) Producing Escherichia coli and Klebsiella spp. Isolates. Türk Mikrobiol Cemiy Derg 46: 88–96.
Oral H, Çolak A, Polat B, Cengiz M, Cengiz S, Baştan A, Kaya S 2014. Sütçü ineklerde subklinik mastitisin tedavisinde aloe vera kullanımının etkinliği. Erciyes Üniv Vet Fak Derg 2014, 11: 157-161.
Özkirim A, Schi̇esser A, Küçüközmen B, İpek A, Sorkun K 2021. Antimicrobial activitiy of oak honey (Quercus spp.) on the pathogen bacteria. Ege Üniv Ziraat Fak Derg 58(2): 100–110.
Parin F N, Terzioğlu P, Parin U, Yeşilyurt A, Eroğlu M, Yıldırım K 2021. Fabrication of polyamide 6/honey/boric acid mats by electrohydrodynamic processes for wound healing applications Polyamide 6/Honey/Boric Acid Bioactive Fibers. Mater Today Commun 102921.
Polat R, Selvi S 2011. A research on bee plants of Edremir (Balıkesir). Harran J of Agri and Food Sci 15(2): 27-32.
Santiago GS, Lasagno MC, Alencar TA 2015. AmpC-lactamase production in Enterobacteria associated with bovine mastitis in Brazil. Afr J Microbiol Res 9: 503-508.
Schmidt M, 2017. Boric acid inhibition of Trichophyton rubrum growth and conidia formation. Biol Trace Elem Res 180(2): 349-354.
Schukken Y, Chuff M, Moroni P, Gurjar A, Santisteban C, Welcome F, Zadoks R 2012) The “other” gram-negative bacteria in mastitis: Klebsiella, Serratia, and more. Vet Clinics: Food Animal Prac 28(2): 239-256.
Sepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M 2000. A Modified Microtiter-Plate Test for Quantification of Staphylococcal Biofilm Formation. J. Microbiol Methods 40(2): 175-179.
Süerdem TB, Akyalçın S, Altan S, Tosun MN 2018. Screening of antimicrobial and antioxidant activity of different types of honey samples obtained from Geyikli (Çanakkale) province. Communications Faculty of Science University of Ankara Series C Biology 27(2): 69–78.
Tepeli S, Zorba N N, 2017. Some properties of raw milk produced in Çanakkale (Yenice) city and subclinical mastitis incidence. Trak Univ J Nat Sci 18: 41-47.
Tepeli̇ SÖ 2020. Origanum onites ve Ocimum basilicum’un blaCTX-M pozitif Enterobacteriaceae üzerine inhibitör etkisi. Çanakkale Onsekiz Mart Üniv Fen Bilimleri Enstit Derg 6: 206–216.
Tepeli SÖ, Eser Ö, Gürpınar Ö, Beşli Y, Zorba NN 2018. Presence of antibiotic resistance genes and heat resistance in Enterobacteriacealesles isolates obtained from cheese production stages. 147-148. In: Proceeding of International XXXVIII. Turkish Microbiology Congress. Antalya, Turkey.
Ulusoy E, Kolayli S, Sarikaya A O 2010. Antioxidant and antimicrobial activity of different floral origin honeys from Türkiye. J Food Biochem 34:321–335.
Valgas C, Souza S M de, Smânia E F A, Smânia Jr A 2007. Screening methods to determine antibacterial activity of natural products. Brazilian J Microbiol 38(2): 369–380.
Wasihun A G, Kasa B G 2016. Evaluation of antibacterial activity of honey against multidrug resistant bacteria in Ayder Referral and Teaching Hospital, Northern Ethiopia. Springer Plus 5(1).
Weston R J 2000. The contribution of catalase and other natural products to the antibacterial activity of honey: A review. Food Chem 71(2): 235–239.
Yalazi E, Zorba M 2020. Antioxidant and antimicrobial properties of honeydew honey of Ida mountains. Turkish J Agri-Food Sci and Tech 8(3): 587-593.
Yıldırım D, Pehlivanoğlu F 2018. Carriage of extended spectrum beta lactamase producing Escherichia coli in calves. FÜ Sag Bil Vet Derg 32: 155-160.

Ayrıntılar

Birincil Dil

İngilizce

Konular

Ziraat, Veterinerlik ve Gıda Bilimleri

Bölüm

Araştırma Makalesi

Yazarlar

Seda Özdikmenli Tepeli ^*
0000-0002-1613-5917
Türkiye

Burcu Kaya
0000-0003-1755-7705
Türkiye

Dilvin İpek
0000-0003-2946-5437
Türkiye

Yayımlanma Tarihi

30 Aralık 2022

Gönderilme Tarihi

14 Temmuz 2021

Kabul Tarihi

10 Şubat 2022

Yayımlandığı Sayı

Yıl 2022 Cilt: 25 Sayı: Ek Sayı 1

DOI

https://doi.org/10.18016/ksutarimdoga.vi.971261

IZ

https://izlik.org/JA26ZG53XC

Kaynak Göster

RIS / Bibtex

APA

Özdikmenli Tepeli, S., Kaya, B., & İpek, D. (2022). Evaluation of Antibacterial Effect of Honey on ESBL and Biofilm-Producing Enterobacterales. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25(Ek Sayı 1), 54-64. https://doi.org/10.18016/ksutarimdoga.vi.971261