Effect of polycaprolactone nanocapsules loaded with essential oils on biofilm formation by Staphylococcus aureus strains isolated from bovine mastitis cases

Authors

  • Gabriela Suthovski Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • Alcione Santa Catarina Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • Diana Paula Perin Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • Rubiana Mara Mainardes Universidade Estadual do Centro Oeste, Guarapuava, Paraná, Brazil
  • Karina Ramirez Starikoff Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • André Lazarin Gallina Universidade Estadual do Centro Oeste, Guarapuava, Paraná, Brazil
  • Maiara Garcia Blagitz Azevedo Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • Fabíola Dalmolin Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil
  • Luciana Velasques Cervo Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil https://orcid.org/0000-0001-7611-1135
  • Dalila Moter Benvegnú Universidade Federal da Fronteira Sul, Realeza, Paraná, Brazil https://orcid.org/0000-0002-3419-9674

DOI:

https://doi.org/10.1590/

Keywords:

Nanoencapsulation;, Citronella;, Melaleuca;, Bovine mastitis;, Biofilm;, Bacteria;, Essential oil

Abstract

Bovine infectious mastitis is largely resistant to antibacterial treatment, mainly due to mechanisms of bacterial resistance in the biofilms formed by Staphylococcus aureus. Melaleuca (MEO) and citronella essential oils (CEO) are promising agents for reducing or eliminating biofilms. Free melaleuca oil presented a medium Minimum Inhibitory Concentration (MIC) of 0.625% and a Minimum Bactericidal Concentration (MBC) of 1.250%, while free citronella oil showed medium MIC and MBC of 0.313%. Thus, free CEO and MEO demonstrate bacteriostatic and bactericidal potential. We generated polymeric nanocapsules containing MEO or CEO and evaluated their efficacy at reducing biofilms formed by S. aureus. Glass and polypropylene spheres were used as test surfaces. To compare the responses of free and encapsulated oils, strains were submitted to 10 different procedures, using free and nanoencapsulated essential oils (EOs) in vitro. We observed no biofilm reduction by MEO, free or nanoencapsulated. However, CEO nanocapsules reduced biofilm formation on glass (p=0.03) and showed a tendency to diminish biofilms on polypropylene (p=0.051). Despite nanoencapsulated CEO reducing biofilms in vitro, the formulation could be improved to modify the CEO component polarity and, including MEO, to obtain more interactions with surfaces and the biofilm matrix.

Downloads

Download data is not yet available.

References

Acosta AC, Silva LBG, Medeiros ES, Pinheiro-Júnior JW, Mota RA. Mastitis in ruminants in Brazil. Pesq Vet Bras. 2016;36:565-573. doi: 10.1590/S0100-736X2016000700001

» https://doi.org/10.1590/S0100-736X2016000700001

Ajose DJ, Oluwarinde BO, Abolarinwa TO, Fri J, Montso KP, Fayemi OE et al. Combating bovine mastitis in the dairy sector in an era of antimicrobial resistance: Ethno-veterinary medicinal option as a viable alternative approach. Front Vet Sci. 2022;9:800322. doi: 10.3389/fvets.2022.800322

» https://doi.org/10.3389/fvets.2022.800322

AOAC. Official methods of analysis. Association of Oficial Analytical Chemists USA, 15.ed. Washington, D.C. 1990, 298p. Available from: https://law.resource.org/pub/us/cfr/ibr/002/aoac.methods.1.1990.pdf

» https://law.resource.org/pub/us/cfr/ibr/002/aoac.methods.1.1990.pdf

Araujo MM, Longo PL. Teste da ação antibacteriana in vitro de óleo essencial comercial de Origanum vulgare (orégano) diante das cepas de Escherichia coli e Staphylococcus aureus Arq Inst Biol (Sao Paulo). 2016;83:1-7. doi: 10.1590/1808-1657000702014

» https://doi.org/10.1590/1808-1657000702014

Araújo EA, Andrade NJ, Carvalho AF, Ramos AM, Silva CAS, Silva LHM. Aspectos coloidais da adesão de micro-organismos. Quim Nova. 2010;33(9):1940-1948. doi: 10.1590/S0100-40422010000900022

» https://doi.org/10.1590/S0100-40422010000900022

Budri PE, Silva NCC, Bonsaglia ECR, Fernandes A, Araújo JP, Doyama JT, et al. Effect of essential oils of Syzygium aromaticum and Cinnamomum zeylanicum and their major components on biofilm production in Staphylococcus aureus strains isolated from milk of cows with mastitis. J Dairy Sci. 2015;98:5899-5904. doi: 10.3168/jds.2015-9442

» https://doi.org/10.3168/jds.2015-9442

Buldain D, Buchamer A V., Marchetti ML, Aliverti F, Bandoni A, Mestorino N. Combination of cloxacillin and essential oil of Melaleuca armillaris as an alternative against Staphylococcus aureus Front Vet Sci. 2018;5:1-8. doi: 10.3389/fvets.2018.00177

» https://doi.org/10.3389/fvets.2018.00177

Carson CF, Mee BJ, Riley TV. Mechanism of Action of Melaleuca alternifolia (Tea Tree) Oil on Staphylococcus aureus Determined by Time-Kill, Lysis, Leakage, and Salt Tolerance Assays and Electron Microscopy. Antimicrob Agents Chemother. 2002;46:1-4. doi: 10.1128/AAC.46.6.1914

» https://doi.org/10.1128/AAC.46.6.1914

CLSI. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. 11th ed. CLSI standard M07. Wayne, PA: CLSI; 2018. Available from: https://clsi.org/media/1928/m07ed11_sample.pdf

» https://clsi.org/media/1928/m07ed11_sample.pdf

Coban AY. Rapid determination of methicillin resistance among Staphylococcus aureus clinical isolates by colorimetric methods. J Clin Microbiol. 2012;50:2191-2193. doi: 10.1128/JCM.00471-12

» https://doi.org/10.1128/JCM.00471-12

Costa CZ, Albuquerque MDCC, Brum MC, Castro AM. Degradação microbiológica e enzimática de polímeros: Uma revisão. Quim Nova. 2015;38:259-267. doi: 10.5935/0100-4042.20140293

» https://doi.org/10.5935/0100-4042.20140293

Deletre E, Chandre F, Williams L, Duménil C, Menut C, Martin T. Electrophysiological and behavioral characterization of bioactive compounds of the Thymus vulgaris, Cymbopogon winterianus, Cuminum cyminum and Cinnamomum zeylanicum essential oils against Anopheles gambiae and prospects for their use as bednet treatments. Parasites Vectors. 2015;8:1-14. doi: 10.1186/s13071-015-0934-y

» https://doi.org/10.1186/s13071-015-0934-y

Duncan B, Li X, Landis RF, Kim ST, Gupta A, Wang LS, et al. Nanoparticle-Stabilized Capsules for the Treatment of Bacterial Biofilms. ACS Nano. 2015;9:7775-7782. doi: 10.1021/acsnano.5b01696

» https://doi.org/10.1021/acsnano.5b01696

Ernst R, Ejsing CS, Antonny B. Homeoviscous Adaptation and the Regulation of Membrane Lipids. J Mol Biol. 2016;428:4776-4791. doi: 10.1016/J.JMB.2016.08.013

» https://doi.org/10.1016/J.JMB.2016.08.013

Feng S, Zhang Y, Fu S, Li Z, Zhang J, Xu Y, et al. Application of Chlorogenic acid as a substitute for antibiotics in Multidrug-resistant Escherichia coli-induced mastitis. Int Immunopharmacol. 2023;114:109536. doi: 10.1016/j. intimp.2022.109536

» https://doi.org/10.1016/j. intimp.2022.109536

Fessi H, Puisieux F, Devissaguet JP, Ammoury N, Benita S. Nanocapsule formation by interfacial polymer deposition following solvent displacement. Int J Pharm.1989;55:1-4. doi: 10.1016/0378-5173(89)90281-0

» https://doi.org/10.1016/0378-5173(89)90281-0

Kim JM, Marshall L, Cornell JA, Preston III JF, Wei CI. Antibacterial Activity of Carvacrol, Citral, and Geraniol against Salmonella typhimurium in Culture Medium and on Fish Cubes. J Food Sci. 1995;60:1364-1368. doi: 10.1111/j.1365-2621.1995.tb04592.x

» https://doi.org/10.1111/j.1365-2621.1995.tb04592.x

Kokina M, Salević A, Kalušević A, Lević S, Pantić M, Pljevljakušić D, et al. Characterization, Antioxidant and Antibacterial Activity of Essential Oils and Their Encapsulation into Biodegradable Material Followed by Freeze-Drying. Food Technol Biotechnol. 2019;57:282-290. doi: 10.17113/ftb.57.02.19.5957

» https://doi.org/10.17113/ftb.57.02.19.5957

Leite BA. Aderência bacteriana e formação de biofilme aos fios de dermossustentação facial. 2008. Dissertação (Mestrado em Bioengenharia) - Bioengenharia, Universidade de São Paulo, São Carlos, 2008. doi: 10.11606/D.82.2008.tde-16102008-115949

» https://doi.org/10.11606/D.82.2008.tde-16102008-115949

Marques SC, Rezende JDGOS, Alves LADF, Silva BC, Alves E, Abreu LR, et al. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Brazilian J Microbiol. 2007;38(3):538-543. doi: 10.1590/S1517-83822007000300029

» https://doi.org/10.1590/S1517-83822007000300029

Martins CR, Lopes WA, Andrade JB. Solubilidade das substâncias orgânicas. Quim Nova. 2013;36(8):1248-1255. doi: 10.1590/S0100-40422013000800026

» https://doi.org/10.1590/S0100-40422013000800026

Melo NFS, Campos EVR, Franz-Montan M, Paula E, Silva CMG, Maruyama CR, et al. Characterization of Articaine-Loaded Poly(ε-caprolactone) Nanocapsules and Solid Lipid Nanoparticles in Hydrogels for Topical Formulations. JNN. 2018;18:4428-4438. doi: 10.1166/jnn.2018.15235

» https://doi.org/10.1166/jnn.2018.15235

Miladi K, Sfar S, Fessi H, Elaissari A. Nanoprecipitation Process: From Particle Preparation to In Vivo Applications. In: Vauthier C, Ponchel G. (eds) Polymer Nanoparticles for Nanomedicines. Springer, Cham. 2016;1:17-53. doi: 10.1007/978-3-319-41421-8_2

» https://doi.org/10.1007/978-3-319-41421-8_2

Notcovich S, DeNicolo G, Flint SH, Williamson NB, Gedye K, Grinberg A, et al. Biofilm-forming potential of Staphylococcus aureus isolated from bovine mastitis in New Zealand. Vet Sci. 2018;5(1):8. doi: 10.3390/vetsci5010008

» https://doi.org/10.3390/vetsci5010008

Oliva A, Costantini S, Angelis M, Garzoli S, Božović M, Mascellino MT, et al. High potency of Melaleuca alternifolia essential oil against multi-drug resistant gram-negative bacteria and methicillin-resistant Staphylococcus aureus Molecules. 2018;23:1-14. doi: 10.3390/molecules23102584

» https://doi.org/10.3390/molecules23102584

Oussalah M, Caillet S, Saucier L, Lacroix M. Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes Food Control. 2007;18:414-420. doi: 10.1016/j.foodcont.2005.11.009

» https://doi.org/10.1016/j.foodcont.2005.11.009

Perez-Lopez MI, Mendez-Reina R, Trier S, Herrfurth C, Feussner I, Bernal A, et al. Variations in carotenoid content and acyl chain composition in exponential, stationary and biofilm states of Staphylococcus aureus, and their influence on membrane biophysical properties. Biochim Biophys Acta Biomembr. 2019;1861:978-987. doi: 10.1016/j.bbamem.2019.02.001

» https://doi.org/10.1016/j.bbamem.2019.02.001

Rigby KM, DeLeo FR. Neutrophils in innate host defense against Staphylococcus aureus infections. Semin Immunopathol. 2012;34:237-259. doi: 10.1007/s00281-011-0295-3

» https://doi.org/10.1007/s00281-011-0295-3

Saporito F, Sandri G, Bonferoni MC, Rossi S, Boselli C, Cornaglia AI, et al. Essential oil-loaded lipid nanoparticles for wound healing. Int J Nanomedicine. 2018;13:175-186. doi: 10.2147/IJN.S152529

» https://doi.org/10.2147/IJN.S152529

Scazzocchio F, Garzoli S, Conti C, Leone C, Renaioli C, Pepi F, et al. Properties and limits of some essential oils: chemical characterisation, antimicrobial activity, interaction with antibiotics and cytotoxicity. Nat Prod Res. 2016;30:1909-1918. doi: 10.1080/14786419.2015.1086346

» https://doi.org/10.1080/14786419.2015.1086346

Sharun K, Dhama K, Tiwari r, Gugjoo MB, Yatoo MI, Patel SK, et al. Advances in therapeutic and managemental approaches of bovine mastitis: a comprehensive review. Vet Q. 2021;41(1):107-136. doi: 10.1080/01652176.2021.1882713

» https://doi.org/10.1080/01652176.2021.1882713

Sikkema J, Bont JAM, Poolman B. Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem. 1994;269:8022-8028. doi: 10.1016/S0021-9258(17)37154-5

» https://doi.org/10.1016/S0021-9258(17)37154-5

Singh S, Fatima Z, Hameed S. Citronellal-induced disruption of membrane homeostasis in Candida albicans and attenuation of its virulence attributes. Rev Soc Bras Med Trop. 2016;49(4):465-472. doi: 10.1590/0037-8682-0190-2016

» https://doi.org/10.1590/0037-8682-0190-2016

Souza ME, Clerici DJ, Verdi CM, Fleck G, Quatrin PM, Spat LE, et al. Antimicrobial activity of Melaleuca alternifolia nanoparticles in polymicrobial biofilm in situ. Microb Pathog. 2017;113:432-437. doi: 10.1016/j.micpath.2017.11.005

» https://doi.org/10.1016/j.micpath.2017.11.005

Stepanović S, Vuković D, Dakić I, Savić B, Ivabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175-179. doi: 10.1016/s0167-7012(00)00122-6

» https://doi.org/10.1016/s0167-7012(00)00122-6

Varela-Ortiz DF, Barboza-Corona JE, González-Marrero J, León-Galván MF, Valencia-Posadas M, Lechuga-Arana AA, et al. Antibiotic susceptibility of Staphylococcus aureus isolated from subclinical bovine mastitis cases and in vitro efficacy of bacteriophage. Vet Res Commun. 2018;42:243-250. doi: 10.1007/s11259-018-9730-4

» https://doi.org/10.1007/s11259-018-9730-4

Yuan YG, Peng QL, Gurunathan S. Effects of silver nanoparticles on multiple drug-resistant strains of Staphylococcus aureus and Pseudomonas aeruginosa from mastitis-infected goats: An alternative approach for antimicrobial therapy. Int J Mol Sci. 2017;18(3):569. doi: 10.3390/ijms18030569

» https://doi.org/10.3390/ijms18030569

Zhang Y, Kong J, Xie Y, Guo Y, Cheng Y, Qian H, et al. Essential oil components inhibit biofilm formation in Erwinia carotovora and Pseudomonas fluorescens via anti-quorum sensing activity. LWT - Food Sci Technol. 2018;92:133-139. doi: 10.1016/j.lwt.2018.02.027

» https://doi.org/10.1016/j.lwt.2018.02.027

Downloads

Published

2023-08-28

Issue

Section

Article

How to Cite

Effect of polycaprolactone nanocapsules loaded with essential oils on biofilm formation by Staphylococcus aureus strains isolated from bovine mastitis cases. (2023). Brazilian Journal of Pharmaceutical Sciences, 59, e23068. https://doi.org/10.1590/