Juniper and immortelle essential oils synergistically inhibit adhesion of nontuberculous mycobacteria to Acanthamoeba castellanii

Peruč, Dolores; Tićac, Brigita; Broznić, Dalibor; Gobin, Ivana

doi:10.2478/aiht-2020-71-3442

Abstract

Acanthamoeba is an opportunistic protozoon, widespread in the aquatic environment, where it can be in endosymbiosis with over 30 pathogenic bacteria, including nontuberculous mycobacteria (NTM). Protozoa play a crucial role in mycobacterial pathogenesis and serve as a reservoir of infection. Since the first step in bacteria making contact with amoebae is adhesion, we were interested in investigating whether essential oils (EOs) can affect it. To that end we investigated the effects of juniper (Juniperus communis) and immortelle (Helichrysum italicum) EOs against Mycobacterium avium, M. intracellulare, and M. gordonae in tap water and against their adhesion to Acanthamoeba castellanii by combining them in synergistic EO concentrations. M. avium and M. intracellulare adhered to A. castellanii to a greater extent than M. gordonae. The adhesion of all NTMs was prevented by the subinhibitory concentrations of EOs. When comparing the effect of synergistic combinations of EOs and the effect of a single concentration from a combination, a higher percentage of adhesion inhibition in all synergistic combinations observed, except against M. gordonae. Neither oil was cytotoxic to A. castellanii. Our findings suggest that the EOs or their components weaken the contact of environmental NTMs and free-living amoebae and indirectly diminish their pathogenic potential, which could be of value in developing strategies for maintenance of water supply systems.

References

Falkinham JO, 3^rd Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 2009;107:356–67. doi: 10.1111/j.1365-2672.2009.04161.x
Open DOI Search in Google Scholar Back to article
De Groote MA, Huitt G. Infections due to rapidly growing mycobacteria. Clin Infect Dis 2006;42:1756–63. doi: 10.1086/504381
Open DOI Search in Google Scholar Back to article
Steed KA, Falkinham JO, 3^rd Effect of growth in biofilms on chlorine susceptibility of Mycobacterium avium and Mycobacterium intracellulare. Appl Environ Microbiol 2006;72:4007–11. doi: 10.1128/AEM.02573-05
Open DOI Search in Google Scholar Back to article
Falkinham JO, 3^rd Mycobacterium avium complex: Adherence as a way of life. AIMS Microbiol 2018;4:428–38. doi: 10.3934/microbiol.2018.3.428
Open DOI Search in Google Scholar Back to article
Falkinham JO, 3^rd Common features of opportunistic premise plumbing pathogens. Int J Environ Res Public Health 2015;12:4533–45. doi: 10.3390/ijerph120504533
Open DOI Search in Google Scholar Back to article
Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 2004;17:413–33. doi: 10.1128/cmr.17.2.413-433.2004
Open DOI Search in Google Scholar Back to article
Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RH. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol Res 2016;193:30–8. doi: 10.1016/j.micres.2016.08.001
Open DOI Search in Google Scholar Back to article
Salah IB, Ghigo E, Drancourt M. Free-living amoebae, a training field for macrophage resistance of mycobacteria. Clin Microbiol Infect 2009;15:894–905. doi: 10.1111/j.1469-0691.2009.03011.x
Open DOI Search in Google Scholar Back to article
Lamrabet O, Mba Medie F, Drancourt M. Acanthamoeba polyphaga-enhanced growth of Mycobacterium smegmatis. PLoS One 2012;7:e29833. doi: 10.1371/journal.pone.0029833
Open DOI Search in Google Scholar Back to article
Cirillo JD, Falkow S, Tompkins LS, Bermudez LE. Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 1997;65:3759–67. PMCID: PMC175536
Search in Google Scholar Back to article
Peruč D, Gobin I, Abram M, Broznić D, Svalina T, Štifter S, Malenica Staver M, Tićac B. Antimycobacterial potential of the juniper berry essential oil in tap water. Arh Hig Rada Toksikol 2018;69:46–54. doi: 10.2478/aiht-2018-69-3085
Open DOI Search in Google Scholar Back to article
Mastelić J, Miloš M, Kuštrak D, Radonić A. Essential Oil and Glycosidically Bound Volatile Compounds from the Needles of Common Juniper Juniperus communis L.). Croat Chem Acta 2000;73:585–93.
Search in Google Scholar Back to article
Sela F, Karapandzova M, Stefkov G, Cvetkovikj I, Kulevanova S. Chemical composition and antimicrobial activity of essential oils of Juniperus excelsa Bieb. (Cupressaceae) grown in R. Macedonia. Pharmacognosy Res 2015;7:74–80. doi: 10.4103/0974-8490.147212
Open DOI Search in Google Scholar Back to article
Angioni A, Barra A, Russo MT, Coroneo V, Dessiä S, Cabras P. Chemical composition of the essential oils of Juniperus from ripe and unripe berries and leaves and their antimicrobial activity. J Agric Food Chem 2003;51:3073–8. doi: 10.1021/jf026203j
Open DOI Search in Google Scholar Back to article
Mastelic J, Politeo O, Jerkovic I. Contribution to the analysis of the essential oil of Helichrysum italicum (Roth) G. Don. Determination of ester bonded acids and phenols. Molecules 2008;13:795–803. doi: 10.3390/molecules13040795
Open DOI Search in Google Scholar Back to article
Bezić N, Vuko E, Ruščić M, Dunkić V. Helichrysum italicum (Roth) G. Don - essential oil composition and activity on tobacco mosaic virus infection. J Plant Physiol Pathol 2016;4:1–3. doi: 10.4172/2329-955X.1000144
Open DOI Search in Google Scholar Back to article
Mancini E, De Martino L, Marandino A, Scognamiglio MR, De Feo V. Chemical composition and possible in vitro phytotoxic activity of Helichrsyum italicum (Roth) Don ssp. italicum. Molecules 2011;16:7725–35. doi: 10.3390/molecules16097725
Open DOI Search in Google Scholar Back to article
Malenica Staver M, Gobin I, Ratkaj I, Petrović M, Vulinović A, Dinarina-Sablić M, Broznić D. In vitro antiproliferative and antimicrobial activity of the essential oil from the flowers and leaves of Helichrysum italicum (Roth) G. Don growing in Central Dalmatia (Croatia). J Essent Oil Bear Pl 2018;21:77–91. doi: 10.1080/0972060X.2018.1433071
Open DOI Search in Google Scholar Back to article
Peruc D, Ticac B, Broznic D, Maglica Z, Sarolic M, Gobin I. Juniperus communis essential oil limit the biofilm formation of Mycobacterium avium and Mycobacterium intracellulare on polystyrene in a temperature-dependent manner. Int J Environ Health Res 2020:1–14. doi: 10.1080/09603123.2020.1741519
Open DOI Search in Google Scholar Back to article
Peruč D, Tićac B, Abram M, Broznić D, Štifter S, Malenica Staver M, Gobin I. Synergistic potential of Juniperus communis and Helichrysum italicum essential oils against nontuberculous mycobacteria. J Med Microbiol 2019;68:703–10. doi: 10.1099/jmm.0.000962
Open DOI Search in Google Scholar Back to article
Doll-Boscardin PM, Sartoratto A, Sales Maia BH, Padilha de Paula J, Nakashima T, Farago PV, Kanunfre CC. In vitro cytotoxic potential of essential oils of Eucalyptus benthamii and its related terpenes on tumor cell lines. Evid Based Complement Alternat Med 2012;2012:342652. doi: 10.1155/2012/342652
Open DOI Search in Google Scholar Back to article
Broznic D, Ratkaj I, Malenica Staver M, Kraljevic Pavelic S, Zurga P, Bubalo D, Gobin I. Evaluation of the antioxidant capacity, antimicrobial and antiproliferative potential of fir Abies alba Mill.) honeydew honey collected from Gorski Kotar (Croatia). Food Technol Biotechnol 2018;56:533–45. doi: 10.17113/ftb.56.04.18.5666
Open DOI Search in Google Scholar Back to article
Gazivoda T, Plevnik M, Plavec J, Kraljevic S, Kralj M, Pavelic K, Balzarini J, De Clercq E, Mintas M, Raic-Malic S. The novel pyrimidine and purine derivatives of L-ascorbic acid: synthesis, one- and two-dimensional ¹H and ¹³C NMR study, cytostatic and antiviral evaluation. Bioorg Med Chem 2005;13:131–9. doi: 10.1016/j.bmc.2004.09.052
Open DOI Search in Google Scholar Back to article
Sarker SD, Nahar L, Kumarasamy Y. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 2007;42:321–4. doi: 10.1016/j.ymeth.2007.01.006
Open DOI Search in Google Scholar Back to article
Andrejak C, Almeida DV, Tyagi S, Converse PJ, Ammerman NC, Grosset JH. Characterization of mouse models of Mycobacterium avium complex infection and evaluation of drug combinations. Antimicrob Agents Chemother 2015;59:2129–35. doi: 10.1128/AAC.04841-14
Open DOI Search in Google Scholar Back to article
Vasiljević B, Knežević-Vučković J, Mitić-Ćulafić D, Orčić D, Francišković M, Srdic-Rajic T, Jovanović M, Nikolić B. Chemical characterization, antioxidant, genotoxic and in vitro cytotoxic activity assessment of Juniperus communis var. saxatilis. Food Chem Toxicol 2018;112:118–25. doi: doi.org/10.1016/j.fct.2017.12.044
Open DOI Search in Google Scholar Back to article
Bassole IH, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012;17:3989–4006. doi: 10.3390/molecules17043989
Open DOI Search in Google Scholar Back to article
White RL, Burgess DS, Manduru M, Bosso JA. Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E test. Antimicrob Agents Chemother 1996;40:1914–8. doi: 10.1128/AAC.40.8.1914
Open DOI Search in Google Scholar Back to article
Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 2016;6:71–9. doi: 10.1016/j.jpha.2015.11.005
Open DOI Search in Google Scholar Back to article
Teanpaisan R, Kawsud P, Pahumunto N, Puripattanavong J. Screening for antibacterial and antibiofilm activity in Thai medicinal plant extracts against oral microorganisms. J Tradit Complement Med 2017;7:172–7. doi: 10.1016/j.jtcme.2016.06.007
Open DOI Search in Google Scholar Back to article
Pfyffer GE, Brown-Elliott BA, Wallace RJJ. Mycobacterium: general characteristics, isolation, and staining procedures. In: Murray PR, editor. Manual of Clinical Microbiology. 8^th editon. Washington, DC: American Society of Microbiology; 2003. p. 532–84.
Search in Google Scholar Back to article
Ovrutsky AR, Chan ED, Kartalija M, Bai X, Jackson M, Gibbs S, Falkinham JO, 3^rd Iseman MD, Reynolds PR, McDonnell G, Thomas V. Cooccurrence of free-living amoebae and nontuberculous Mycobacteria in hospital water networks, and preferential growth of Mycobacterium avium in Acanthamoeba lenticulata. Appl Environ Microbiol 2013;79:3185–92. doi: 10.1128/AEM.03823-12
Open DOI Search in Google Scholar Back to article
Miltner EC, Bermudez LE. Mycobacterium avium grown in Acanthamoeba castellanii is protected from the effects of antimicrobials. Antimicrob Agents Chemother 2000;44:1990–4. doi: 10.1128/aac.44.7.1990-1994.2000
Open DOI Search in Google Scholar Back to article
Ohno A, Kato N, Sakamoto R, Kimura S, Yamaguchi K. Temperature-dependent parasitic relationship between Legionella pneumophila and a free-living amoeba Acanthamoeba castellanii Appl Environ Microbiol 2008;74:4585–8. doi: 10.1128/AEM.00083-08
Open DOI Search in Google Scholar Back to article
Khan NA. Acanthamoeba biology and increasing importance in human health. FEMS Microbiol Rev 2006;30:564–95. doi: 10.1111/j.1574-6976.2006.00023.x
Open DOI Search in Google Scholar Back to article
Berry D, Horn M, Xi C, Raskin L. Mycobacterium avium infections of Acanthamoeba strains: host strain variability, grazing-acquired infections, and altered dynamics of inactivation with monochloramine. Appl Environ Microbiol 2010;76:6685–8. doi: 10.1128/AEM.00644-10
Open DOI Search in Google Scholar Back to article
Mackowiak PA, Marling-Cason M, Cohen RL. Effects of temperature on antimicrobial susceptibility of bacteria. J Infect Dis 1982;145:550–3. doi: 10.1093/infdis/145.4.550
Open DOI Search in Google Scholar Back to article

Juniper and immortelle essential oils synergistically inhibit adhesion of nontuberculous mycobacteria to Acanthamoeba castellanii

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