1887

Abstract

Bovine mastitis is a costly disease in the dairy industry and does not always respond to antibiotic treatment. The major components of terpeneless, cold-pressed Valencia orange oil – citral, linalool, decanal and valencene – were examined as potential alternative treatments for associated mastitis. The minimum inhibitory concentration (MIC) of all four components against was determined after incubation for 24 h. Growth inhibition assays were performed for all effective components on for either a 3 h or 72 h treatment. These components were tested for the ability to disrupt pre-formed biofilms after 24 h of treatment by measuring absorbance at 540 nm. Cytotoxicity against immortalized bovine mammary epithelial (MAC-T) cells was measured using an MTT assay following a 1 h exposure. Only concentrations below the 50 % cytostatic concentration (CC50) were used in an adherence and invasion assay of on MAC-T cells, and for measurements of virulence and biofilm gene expression via qPCR. The MICs of citral and linalool were 0.02 % and 0.12 %, respectively, but decanal and valencene were ineffective. Citral and linalool were capable of inhibiting growth of after 24 h at their MIC values and inhibited pre-formed biofilms of . The concentrations below the CC50 were 0.02 % for citral and 0.12 % for linalool. These concentrations inhibited the adhesion and invasion ability of and downregulated virulence genes. Only 0.12 % linalool downregulated the expression of biofilm-forming genes. These components should be considered for further study.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000286
2016-07-01
2020-04-05
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/7/688.html?itemId=/content/journal/jmm/10.1099/jmm.0.000286&mimeType=html&fmt=ahah

References

  1. Ahn J., Kim S., Jung L., Biswas D.. 2014; Effect of bacteriophage on the translational and transcriptional expression of inflammatory mediators in chicken macrophage. J Poultry Sci51:96–103[Crossref]
    [Google Scholar]
  2. Alzoreky N. S., Nakahara K.. 2003; Antibacterial activity of extracts from some edible plants commonly consumed in Asia. Int J Food Microbiol80:223–230[PubMed][Crossref]
    [Google Scholar]
  3. Atshan S. S., Shamsudin M. N., Karunanidhi A., van Belkum A., Lung L. T., Sekawi Z., Nathan J. J., Ling K. H., Seng J. S. et al. 2013; Quantitative PCR analysis of genes expressed during biofilm development of methicillin resistant Staphylococcus aureus (MRSA). Infect Genet Evol18:106–112 [CrossRef][PubMed]
    [Google Scholar]
  4. Bar D., Tauer L. W., Bennett G., González R. N., Hertl J. A., Schukken Y. H., Schulte H. F., Welcome F. L., Gröhn Y. T.. 2008; The cost of generic clinical mastitis in dairy cows as estimated by using dynamic programming. J Dairy Sci91:2205–2214 [CrossRef][PubMed]
    [Google Scholar]
  5. Barkema H. W., Schukken Y. H., Zadoks R. N.. 2006; Invited Review: The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci89:1877–1895 [CrossRef][PubMed]
    [Google Scholar]
  6. Barlow J.. 2011; Mastitis therapy and antimicrobial susceptibility: a multispecies review with a focus on antibiotic treatment of mastitis in dairy cattle. J Mammary Gland Biol Neoplasia16:383–407 [CrossRef][PubMed]
    [Google Scholar]
  7. Biswas D., Itoh K., Sasakawa C.. 2000; Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol29:203–211[PubMed][Crossref]
    [Google Scholar]
  8. Burman J. D., Leung E., Atkins K. L., O'Seaghdha M. N., Lango L., Bernadó P., Bagby S., Svergun D. I., Foster T. J. et al. 2008; Interaction of human complement with Sbi, a Staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J Biol Chem283:17579–17593 [CrossRef][PubMed]
    [Google Scholar]
  9. Contreras G. A., Rodríguez J. M.. 2011; Mastitis: comparative etiology and epidemiology. J Mammary Gland Biol Neoplasia16:339–356 [CrossRef][PubMed]
    [Google Scholar]
  10. de Carvalho C. C., da Fonseca M. M.. 2007; Preventing biofilm formation: promoting cell separation with terpenes. FEMS Microbiol Ecol61:406–413 [CrossRef][PubMed]
    [Google Scholar]
  11. Downer R., Roche F., Park P. W., Mecham R. P., Foster T. J.. 2002; The elastin-binding protein of Staphylococcus aureus (EbpS) is expressed at the cell surface as an integral membrane protein and not as a cell wall-associated protein. J Biol Chem277:243–250 [CrossRef][PubMed]
    [Google Scholar]
  12. Fisher K., Phillips C. A.. 2006; The effect of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J Appl Microbiol101:1232–1240 [CrossRef][PubMed]
    [Google Scholar]
  13. Götz F.. 2002; Staphylococcus and biofilms. Mol Microbiol43:1367–1378[PubMed][Crossref]
    [Google Scholar]
  14. Harmon R. J.. 1994; Physiology of mastitis and factors affecting somatic cell counts. J Dairy Sci77:2103–2112 [CrossRef][PubMed]
    [Google Scholar]
  15. Haveri M., Taponen S., Vuopio-Varkila J., Salmenlinna S., Pyörälä S.. 2005; Bacterial genotype affects the manifestation and persistence of bovine Staphylococcus aureus intramammary infection. J Clin Microbiol43:959–961 [CrossRef][PubMed]
    [Google Scholar]
  16. Hayes A. J., Markovic B.. 2002; Toxicity of Australian essential oil Backhousia citriodora (Lemon myrtle). Part 1. Antimicrobial activity and in vitro cytotoxicity. Food Chem Toxicol40:535–543 [CrossRef][PubMed]
    [Google Scholar]
  17. Heinrichs J. H., Gatlin L. E., Kunsch C., Choi G. H., Hanson M. S.. 1999; Identification and characterization of SirA, an iron-regulated protein from Staphylococcus aureus . Genet. Mol. Biol181:1436–1443
    [Google Scholar]
  18. Houston P., Rowe S. E., Pozzi C., Waters E. M., O'Gara J. P.. 2011; Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun79:1153–1165 [CrossRef][PubMed]
    [Google Scholar]
  19. Karaolis D. K., Rashid M. H., Chythanya R., Luo W., Hyodo M., Hayakawa Y.. 2005; c-di-GMP (3'-5'-cyclic diguanylic acid) inhibits Staphylococcus aureus cell-cell interactions and biofilm formation. Antimicrob Agents Chemother49:1029–1038 [CrossRef][PubMed]
    [Google Scholar]
  20. Kim J., Marshall M. R., Wei C.. 1995; Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem43:2839–2845[Crossref]
    [Google Scholar]
  21. Kuźma Ł., Rózalski M., Walencka E., Rózalska B., Wysokińska H.. 2007; Antimicrobial activity of diterpenoids from hairy roots of Salvia sclarea L.: salvipisone as a potential anti-biofilm agent active against antibiotic resistant Staphylococci. Phytomedicine14:31–35 [CrossRef][PubMed]
    [Google Scholar]
  22. Lis-Balchin M., Deans S. G.. 1997; Bioactivity of selected plant essential oils against Listeria monocytogenes . J Appl Microbiol82:759–762[PubMed][Crossref]
    [Google Scholar]
  23. Liu K., Chen Q., Liu Y., Zhou X., Wang X.. 2012; Isolation and biological activities of decanal, linalool, valencene, and octanal from sweet orange oil. J Food Sci77:C1156–C1161 [CrossRef][PubMed]
    [Google Scholar]
  24. Ma Y., Xu Y., Yestrepsky B. D., Sorenson R. J., Chen M., Larsen S. D., Sun H.. 2012; Novel inhibitors of Staphylococcus aureus virulence gene expression and biofilm formation. PLoS One7:e47255 [CrossRef][PubMed]
    [Google Scholar]
  25. Makovec J. A., Ruegg P. L.. 2003; Results of milk samples submitted for microbiological examination in Wisconsin from 1994 to 2001. J Dairy Sci86:3466–3472 [CrossRef][PubMed]
    [Google Scholar]
  26. Mubarak E. E., Ali L. Z., Ahmed I. F. A., Ahmed A. B. A., Taha R. M.. 2015; Essential oil compositions and cytotoxicity from various organs of Eucalyptus camaldulensis . Int J Agric Biol17:320–326
    [Google Scholar]
  27. Muthaiyan A., Martin E. M., Natesan S., Crandall P. G., Wilkinson B. J., Ricke S. C.. 2012; Antimicrobial effect and mode of action of terpeneless cold-pressed Valencia orange essential oil on methicillin-resistant Staphylococcus aureus . J Appl Microbiol112:1020–1033 [CrossRef][PubMed]
    [Google Scholar]
  28. Nannapaneni R., Chalova V. I., Crandall P. G., Ricke S. C., Johnson M. G., O'Bryan C. A.. 2009; Campylobacter and Arcobacter species sensitivity to commercial orange oil fractions. Int J Food Microbiol129:43–49 [CrossRef][PubMed]
    [Google Scholar]
  29. National Mastitis Council 1996; Current Concepts in Bovine Mastitis Madison WI: Natl. Mast Coun;
    [Google Scholar]
  30. O'Gara J. P.. 2007; ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus . FEMS Microbiol Lett270:179–188 [CrossRef][PubMed]
    [Google Scholar]
  31. O'Toole G. A.. 2011; Microtiter dish biofilm formation assay. J Vis Exp47: [CrossRef][PubMed]
    [Google Scholar]
  32. Ott S.. 1999; Costs of herd-level production losses associated with subclinical mastitis in US Dairy Cows. In Proceedings of the 38th Annual Meeting of National Mastitis Council , pp.152–156 Arlington VA: Natl. Mast Coun. Madison WI;
    [Google Scholar]
  33. Prashar A., Locke I. C., Evans C. S.. 2004; Cytotoxicity of lavender oil and its major components to human skin cells. Cell Prolif37:221–229 [CrossRef][PubMed]
    [Google Scholar]
  34. Reyher K. K., Haine D., Dohoo I. R., Revie C. W.. 2012; Examining the effect of intramammary infections with minor mastitis pathogens on the acquisition of new intramammary infections with major mastitis pathogens--a systematic review and meta-analysis. J Dairy Sci95:6483–6502 [CrossRef][PubMed]
    [Google Scholar]
  35. Saddiq A., Khayyat S.. 2010; Chemical and antimicrobial studies of monoterpene: Citral. Pest. Biochem. Physiol98:89–93[Crossref]
    [Google Scholar]
  36. Salaheen S., Almario J. A., Biswas D.. 2014a; Inhibition of growth and alteration of host cell interactions of Pasteurella multocida with natural byproducts. Poult Sci93:1375–1382 [CrossRef][PubMed]
    [Google Scholar]
  37. Salaheen S., Nguyen C., Hewes D., Biswas D.. 2014b; Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni . Food Control46:174–181 [CrossRef]
    [Google Scholar]
  38. Smith-Palmer A., Stewart J., Fyfe L.. 1998; Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett Appl Microbiol26:118–122 [CrossRef][PubMed]
    [Google Scholar]
  39. Ster C., Gilbert F. B., Cochard T., Poutrel B.. 2005; Transcriptional profiles of regulatory and virulence factors of Staphylococcus aureus of bovine origin: oxygen impact and strain-to-strain variations. Mol Cell Probes19:227–235 [CrossRef][PubMed]
    [Google Scholar]
  40. Trivier D., Courcol R. J.. 1996; Iron depletion and virulence in Staphylococcus aureus . FEMS Microbiol Lett141:117–127 [CrossRef][PubMed]
    [Google Scholar]
  41. Wilson D. J., Gonzalez R. N., Das H. H.. 1997; Bovine mastitis pathogens in New York and Pennsylvania: prevalence and effects on somatic cell count and milk production. J Dairy Sci80:2592–2598 [CrossRef][PubMed]
    [Google Scholar]
  42. Yang H., Hewes D., Salaheen S., Federman C., Biswas D.. 2014; Effects of blackberry juice on growth inhibition of foodborne pathogens and growth promotion of Lactobacillus . Food Control37:15–20 [CrossRef]
    [Google Scholar]
  43. Yousefzadi M., Heidari M., Akbarpour M., Mirjalili M. H., Zeinali A., Parsa M.. 2011; In vitro cytotoxic activity of the essential oil of Dorema ammoniacum D.Don. Middle-East. J Sci Res7:511–514
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000286
Loading
/content/journal/jmm/10.1099/jmm.0.000286
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error