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Biofilm Degradation of Nontuberculous Mycobacteria processes Article Biofilm Degradation of Nontuberculous Mycobacteria Formed on Stainless Steel Following Treatment with Immortelle (Helichrysum italicum) and Common Juniper (Juniperus communis) Essential Oils Dolores Peruˇc 1,* , Dalibor Brozni´c 2 , Željka Maglica 3, Zvonimir Marijanovi´c 4, Ljerka Karleuša 5 and Ivana Gobin 1 1 Department of Microbiology and Parasitology, Faculty of Medicine, University of Rijeka, 51000 Rijeka, Croatia; [email protected] 2 Department of Medical Chemistry, Biochemistry and Clinical Chemistry, Faculty of Medicine, University of Rijeka, 51000 Rijeka, Croatia; [email protected] 3 Department of Biotechnology, University of Rijeka, 51000 Rijeka, Croatia; [email protected] 4 Department of Food Technology and Biotechnology, Faculty of Chemistry and Technology, University of Split, 21000 Split, Croatia; [email protected] 5 Department of Physiology and Immunology, Faculty of Medicine, University of Rijeka, 51000 Rijeka, Croatia; [email protected] * Correspondence: [email protected]; Tel.: +385-(0)51-651-145; Fax: +385-(0)51-651-177 Abstract: Nontuberculous mycobacteria, like other opportunistic premise plumbing pathogens, pro- duce resistant biofilms on various surfaces in the plumbing system including pipes, tanks, and fittings. Citation: Peruˇc,D.; Brozni´c,D.; Since standard methods of water disinfection are ineffective in eradicating biofilms, research into new Maglica, Ž.; Marijanovi´c,Z.; Karleuša, agents is necessary. Essential oils (EOs) have great potential as anti-biofilm agents. Therefore, the pur- L.; Gobin, I. Biofilm Degradation of pose of this research was to investigate the potential anti-biofilm effect of common juniper (Juniperus Nontuberculous Mycobacteria communis) and immortelle (Helichrysum italicum) EOs. Minimum inhibitory concentrations (MIC), Formed on Stainless Steel Following Treatment with Immortelle minimum bactericidal concentrations (MBC), and minimum effective concentrations of EOs on My- (Helichrysum italicum) and Common cobacterium avium, M. intracellulare, and M. gordonae were tested. Additionally, biofilms on the surface Juniper (Juniperus communis) Essential of a stainless steel disc were treated with single or mixed concentration of EOs, in order to investigate Oils. Processes 2021, 9, 362. https:// their degeneration via the bacterial count and confocal laser scanning microscopy (CLSM). H. italicum doi.org/10.3390/pr9020362 EO showed the strongest biofilm degradation ability against all Mycobacteria strains that were tested. The strongest effect in the biofilm degradation after the single or mixed applications of EOs was Academic Editors: Nicola Gargiulo observed against M. gordonae, followed by M. avium. The most resistant was the M. intracellulare and Elwira Sieniawska biofilm. Synergistic combinations of J. communis and H. italicum EOs therefore seem to be an effective Received: 30 December 2020 substance in biofilm degradation for use in small water systems such as baths or hot tubs. Accepted: 10 February 2021 Published: 16 February 2021 Keywords: biofilm; common juniper; immortelle; nontuberculous mycobacteria; stainless steel Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Mycobacteria originated 150 million years ago [1]. The genus Mycobacterium is the only member of the family Mycobacteriaceae from the order Actinomycetales and the class Actinomycetes. Today, more than 200 species belong to the genus Mycobacterium, which include obligate and opportunistic pathogens and saprophytes [2]. Nontuberculous my- Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. cobacteria (NTM) are a heterogeneous group of environmental bacteria mainly isolated This article is an open access article from water, soil, dust, various animals, milk, and dairy products [3]. Although mostly ap- distributed under the terms and athogenic, nowadays, they increasingly represent important environmental opportunistic conditions of the Creative Commons pathogens [4]. Mycobacterium avium and M. intracellulare are members of the Mycobacterium Attribution (CC BY) license (https:// avium complex (MAC). These are slow-growing unpigmented mycobacteria that form creativecommons.org/licenses/by/ smooth, flat, transparent colonies. MACs are the most frequently isolated pathogenic NTM 4.0/). species from respiratory samples [5]. M. gordonae is a mycobacterium that forms smooth Processes 2021, 9, 362. https://doi.org/10.3390/pr9020362 https://www.mdpi.com/journal/processes Processes 2021, 9, 362 2 of 17 orange colonies and is a mostly apathogenic, saprophytic species of NTM [5,6]. In Croatia, it is one of the most common isolates from the respiratory tract, but is extremely rarely associated with clinically proven infection [7]. Inhalation of infectious aerosol is a major transmission route for pulmonary infections caused by NTM [8]. The source of infection can be drinking tap water, well water, taps in residential, hospital and laboratory areas, hot tub water, house dust, potted soil, forest soil, domestic animals, or sea water [8–10]. The presence of NTM in these sources is mainly a result of their ability to form biofilms and to survive in free-living amoebae [9]. Due to a high content of complex lipids and mycolates, the cell wall of mycobacteria is extremely hydrophobic, which greatly facilitates their binding to various surfaces and biofilm formation and contributes to their resistance to phagocytosis, disinfectants, and antimicrobial drugs [2]. The research revealed that tap wa- ter is often a source of NTM colonization and/or infection [11]. In the aquatic environment, M. avium has an exceptional ability to form biofilm [4]. As a result, this mycobacterium, along with Legionella pneumophila, Pseudomonas aeruginosa, and Acinetobacter baumannii, is classified as an opportunistic premise plumbing pathogen (OPPP) [12]. Twice as many Mycobacterium spp. were found in biofilm samples from showerheads than were found in drinking water samples. M. gordonae, M. avium, M. intracellulare, and M. xenopi were the species most frequently isolated from these biofilms, while drinking water contained significant amounts of M. gordonae, M. chelonae, M. fortuitum, and M. terrae [13,14]. Most studies comparing the formation of biofilms of slow-growing NTMs in the aquatic environment have identified three key determinants: First, NTMs can, indepen- dently, without the presence of other microorganisms, create a suitable substrate and begin biofilm formation. Second, plastic and siliconized substrates widely used in medicine and in the water supply system can be very quickly colonized with mycobacteria. Third, NTMs can produce biofilms under the conditions of low nutrient levels such as in the water supply system, without significantly impairing their growth potential [15]. The Mediterranean area is known as the natural habitat of a large number of medicinal plants that have long been utilized in traditional medicine. According to the available data, the Croatian flora consists of over 4000 species [16]. Research on the antimicrobial effect of certain plant species and natural substances, the effective concentration of which has no harmful effects on the human body, represents an important contribution to the improvement of therapeutic and preventive protocols. The biochemical and physiological properties of each plant species directly depend on its chemical composition. This primarily refers to the fact that each individual species inhabiting a particular geographical area will have a genome encoding specific enzyme system, which in turn produces a specific range of certain chemical compounds [17]. Essential oils (EO) are extracts characterized as a complex mixture of volatile constituents having a strong scent. They are formed by the secondary metabolism of plants [18]. There is substantial data in the literature on the antibacterial, antifungal, and antiviral effects of different EOs [19–21], but few studies have been made on the effects of EOs on mycobacteria [22,23]. Common juniper (Juniperus communis) is an evergreen coniferous shrub that grows in the hilly regions of the Northern Hemisphere. Its needles and dried fruit are used in traditional medicine as diuretic, uroantiseptic, carminative, digestive, and antioxidant agents [24]. The main bioactive substances in J. communis EO are: a- and b-pinene, b- myrcene, sabinene, limonene, terpinene-4-ol and b-caryophyllene [25–27]. Immortelle (Helichrysum italicum), a perennial flowering plant belonging to the genus Helichrysum, from the family Asteraceae, is widely distributed along the Adriatic coast and islands and is used in traditional medicine for its anti-inflammatory, antimicrobial, and antioxidant properties [28]. H. italicum EO, produced from the flowering plant, is most commonly reported to contain: a-pinene, neryl acetate, b-curcumene, g-curcumene, b-caryophyllene, limonene, a-cadrene, and geranyl acetate [17,29,30]. The first aim of this study was to determine the chemical compositions of J. communis and H. italicum EOs as well as to examine the antimicrobial effects of these EOs on M. avium, M. intracellulare, and M.gordonae and to determine their minimum inhibitory concentration Processes 2021, 9, 362 3 of 17 (MIC) and minimum bactericidal concentration (MBC). The second aim was to examine the interaction of J. communis and H. italicum EOs on selected NTMs and their effect on the degradation of mycobacterial biofilms
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