Summarized antibiofilm activity of EOs against MDR
Abstract
Staphylococcus aureus is one of the most common pathogens that cause recurrent, chronic, and biofilm-related diseases. Biofilms are the major form of bacterial structures capable of secreting polysaccharides that provide intrinsic protection against environmental stress like high concentrations of antibiotics. This, along with the emergence of multidrug-resistant strains, has made S. aureus infections a worldwide problem as a result of the inefficiency of the conventional medications. Plant essential oils (EOs) are an important source for drug discovery and pharmaceutical development due to their diverse biological activities, such as antimicrobial agents. The EOs’ microbicide action is extensively reported at the scientific literature and frequently associated with bioactive molecules, such as aldehydes and terpenes. However, the ability of some EOs to inhibit biofilm formation has been poorly explored and it is still unclear how they could be applied in specific treatments against well-known infections. Therefore, this chapter will address virulence factors and biofilm formation of S. aureus, as well as bioprospecting of essential oil as a promising source in the search for new bioactive compounds employed in the fight against this microorganism.
Keywords
- antibiofilm activity
- biofilm-related diseases
- essential oil
- natural products
- Staphylococcus aureus
1. Introduction
The emergence of multidrug-resistant (MDR) bacteria is correlated with selective pressure caused by the indiscriminate use of antibiotics, which reduces therapeutic options available [1]. Consequently, it leads to a serious public health problem frequently associated with increase of healthcare costs and high morbimortality rates [2]. One worldwide recognized bacterial pathogen with the ability to develop severe clinical conditions such as pneumonia and septicemia is
Recently, the use of natural compounds, such as EOs obtained from different parts of the plants, is receiving attention for their biological activities, including antioxidant, anti-inflammatory, and anticancer effect [8]. Moreover, EOs have been frequently mentioned on scientific literature as a promising antimicrobial agent, being effective against a wide range of pathogenic bacteria and yeast [9, 10]. Thus, this chapter will present a comprehensive overview about general features of
2. Staphylococcus aureus
2.1 Clinical relevance and virulence factors
Member of the
Widely disseminated in nature,
Bacterial sepsis confirmed by blood cultures in pediatric hospitals, Gram-positive bacteria (62%) were involved in most of the infection cases. Among them, the major reported strains were
The bacterial adherence to extracellular matrix cells in the host is one of the most important steps for colonization. It is mediated mainly by surface-anchored proteins classified as MSCRAMM (microbial surface components recognizing adhesive matrix molecules) family. Among them, two fibronectin binding proteins, FnbA and FnbB, contribute considerably to epithelial tissue colonization in various pathological manifestations and medical device-related infections [31]. Other cell surface protein related in adhesion mechanisms are named clumping factor A and B (ClfA and ClfB). The first one has a highlighted ability to interact with soluble proteins, fibrinogen, and fibrin, present in blood plasma. These surface components aid the microorganism to interact with plasma protein-coated biomaterials and, consequently, make possible the colonization and biofilm formation on medical devices [32]. The ClfB is frequently associated to nasal colonization due to high affinity to cornified envelope of the nostrils, which promotes the formation of skin abscesses by binding to the protein loricrin [33]. It is worth mentioning genes capable of encoding proteins on the cell surface,
2.2 Antibiotic resistance and biofilm formation
Historically, infections caused by MDR
Subsequently, vancomycin was used as an alternative to cases of MRSA infection [40]. However, the constant use of this antibiotic leads to the emergence of vancomycin-resistant
Furthermore, the ability of some microorganisms to form cellular agglomerates, such as biofilms, contributes way more for antibiotic resistance. In summary, biofilm is a three-dimensional community of microorganisms covered and embedded in a self-produced matrix of extracellular polymeric substances (EPS) [44]. Such multicellular structure provides intrinsic protection for biofilm-embedded cells against hostile environments, for instance extreme temperature and pH, high salinity and pressure, poor nutrients, and antibiotics [45–47]. Microorganisms that grow on biofilms often exhibited different physiology profile from planktonic cells, especially in terms of their response to antibiotic treatment [48]. Although biofilm lifestyle can arise from a single cell, differential environmental conditions throughout the community can potentiate the development of distinct subpopulations. Gradients in oxygen, nutrients, and electron acceptors can cause heterogeneous gene expression throughout a biofilm. This communication between these bacterial cells, called quorum sensing, mediated the genes expression and activate virulence factors [49].
Thus, several steps regarding biofilm formation of
3. Essential oils
3.1 General aspect
Essential oils are compounds obtained from the secondary metabolism of the plants. They are characterized as complex mixtures of volatile compounds abundant in aromatic plants found in different parts of the plant, including leaves, flowers, stem, roots, seeds, and fruits [59]. There is a diversity of these substances described in the literature in commercial use, such as in perfumes, pharmaceuticals, cosmetics, insecticides, and food additives [60].
Generally, they are oily-looking liquids at room temperature of complex mixtures of volatile lipophilic substances, usually with pleasant scent. In water, EOs have a limited solubility, which allows their separation by steam or water distillation. Other methods to obtain EOs include cold-press extraction used for citrus peels, separation by solubility using organic solvents, and through supercritical fluid extraction [61]. They are usually unstable against environmental factors such as light, temperature, water activity, and salinity, affecting their constitution, contributing to the appearance of chemotypes with particular compositions. Depending on the technique used in the course of a separation, reactions such as ester hydrolysis, autoxidation, and rearrangements may occur, leading to the formation of artifacts and modifying their biological activity [62].
Compounds included in the EOs are produced in the cytoplasm and plastids of plant cells through the action of terpene synthase enzymes (TPSs), in which they use substrates from two pathways involved in the synthesis of terpenes: the mevalonate (MVA) and the methyl-eritritol phosphate (MEP) pathways [63]. They are localized and stored in complex secretory structures, such as glands, secretory cavities, hairs or trichomes, epidermal cells, internal secretory cells, and the secretory pockets [64]. Many of these substances are now known to be directly involved in the defense or attraction mechanisms of plants and often show interesting biological activities [65].
Despite containing two or three main components at a level of 20–70%, EOs are very complex mixtures of substances. In general, the majority components are formed by terpenes and phenylpropanoids [66]. In the very first definitions of EOs, these were frequently identified with terpenes, principally mono- and sesquiterpenes. Other substances have also been identified as alcohols, aldehydes, ketones, phenols, esters, ethers, oxides, peroxides, furans, organic acids, lactones, coumarins, sulfur compounds, anthraquinones, and alkaloids [61]. In the mixture, such compounds come in different concentrations. Usually, one of them is the majority compound, with others in lower grades and some in very low quantities (trace). EOs are composed of volatile hydrocarbons, and they may contain oxygen, sulfur, and halogens (rare) in their chemical structure [67]. In a reduced number of species, the predominant components are aromatic molecules, and these include thyme (thymol and carvacrol), peppermint (menthol), and anise (anethol) [68].
3.2 Antimicrobial and antibiofilm potential
Humans have used EOs for thousands of years, not only as aromatic extracts and for beauty care and culinary uses, but also in folk medicine, due to their many different pharmacological activities, such as antiseptic, anti-inflammatory, and analgesic properties [65]. Some of the EOs, and their components, have demonstrated the relevant antimicrobial potential against a wide range of microbial pathogens [69]. Additionally, Gram-positive bacteria, such as
The broad-spectrum activity of EOs is related to the diverse chemical reactions of aldehydes, phenolic compounds, and terpenes, synthesized from secondary metabolism by different plant parts [10]. The EO action is attributed to the ability of their constituents to interact with the cell membrane and consequently disturb the microbial integrity, leading to cell death [72]. However, EO bioactive components can have several cellular targets, and they are mainly associated with cytoplasmic coagulation, inhibition of ATP-production enzymes, alteration in ion transport, cell-wall damage, and bacterial membrane destruction (Figure 3) [73].
The emergence of MRD pathogens has caused an interesting shift from the onerous development of novel classes of antibiotics to the more straightforward application of synergism or combinatory therapy in the hope of reviving the efficacy and effectiveness of existing antibiotics [74]. Several studies have demonstrated that there was synergetic effect when two or more EOs are mixed together. Moreover, there are also reports of synergistic activity of EOs when used in combination with well-known antibiotics. When blended with other antimicrobial agents, the constituents of EOs can unlock the cell membrane channels, thus opening the passage of antimicrobial agents to reach their target sites [75].
The capacity of some EOs to inhibit biofilm formation has been less explored; however, some reports suggested their utilization as potent inhibitor of virulence factors and biofilm formation [76]. So far, a plethora of potential antibiofilm agents, mainly inspired by natural products, has been developed and shown great promise in either facilitating the dispersion of preformed biofilms or inhibiting the formation of new biofilms
Table 1 shows some studies based on the
Scientific name | Plant part | Major chemical compounds | Resistant phenotype | Ref. |
---|---|---|---|---|
|
Aerial | 1,8 Cineole, methyl chavicol, camphor | MRSA, MRSAMupR | [79] |
|
Aerial | Methyl chavicol, methyl eugenol | MRSA, MRSAMupR | [79] |
|
Aerial | Camphor, 1,8-cineole | MRSA, MRSAMupR | [79] |
|
Aerial | 1,8-cineole, methyl chavicol, camphor | MRSA, MRSAMupR | [79] |
|
Bark and leaves | Cinnamaldehyde | MRSA | [80] |
|
Fruit | Ethanolic compounds | MSSA MRSAMupR | [80] |
|
Leaves | Eugenol, cinnamaldehyde, citral, geraniol | MSSA, MRSA | [80, 81] |
|
Aerial | Eucalyptol, [+] spathulenol, α-pinene | MRSA, MSSA | [82] |
|
Aerial | Geranial, neral | MSSA | [83] |
|
Aerial | Menthol, menthone, menthyl acetate | MRSA, MSSA | [84] |
|
Aerial | α-Terpineol, terpinen-4-ol | MSSA | [85] |
|
Leaves | Eugenol, α-terpineol, γ-terpinene | MSSA | [86] |
|
Leaves | Eugenol, 1,8-cineole | MRSA, MSSA | [87] |
|
Leaves and Arial | 1-Terpineol, sabinene, γ-terpinene | MRSA, MSSA | [88, 89] |
|
Leaves | Limonene, sabinene, β-pinene | MSSA | [90] |
|
Leaves and flower | 1,8-cineol, camphor, α-pinene | MSSA | [91] |
|
Leaves | β-cubebene, limonene, α-pinene | MSSA, MRSA | [92] |
|
Leaves | Carvacrol, p-cymene, δ-terpinene | MRSA | [93] |
|
Aerial | Eugenol, caryophyllene | MSSA | [90] |
|
Aerial | p-Cymene, γ-terpinene | MRSA, MSSA | [82, 94] |
|
Aerial | Carvacrol, γ-terpinene | MSSA | [92] |
|
Leaves | Thymol, carvacrol, rho-cymene | MRSA, MSSA | [95] |
Antibiofilm agents can have different therapeutic applications depending on their effects on the biofilm: compounds that interfere with biofilm formation could be exploited in the prophylaxis of implant surgery or for the coatings in medical devices, whereas agents able to disperse biofilm structure could be administered in combination with conventional antibiotics for the treatment of biofilm-associated infections [96]. Despite the growing number of new potent EO-based antibiofilm compounds described, there is still a great challenge in the development of antibiofilm drugs. Once the EO compounds, which has such activity, discovered so far need further optimizations to improve potency for it become one clinical candidate for such approach. Other EO features such as stability, volatility, encapsulation, and optimal dosage should be considered for the development of EO-based antibiofilm drugs. However, it is expected that in the coming years some of these compounds would be translated into antibiofilm drugs.
4. Conclusion
Due to the emergence of multiresistant strains and biofilm formation, there is an urgent need to find effective alternatives against
References
- 1.
Karam G, Chastre J, Wilcox MH, Vincent JL. Antibiotic strategies in the era of multidrug resistance. Critical Care. 2016; 20 (1):1-9 - 2.
Van DD, Paterson DL. Multidrug-resistant bacteria in the community: Trends and lessons learned. Infectious Disease Clinics of North America. 2016; 30 (2):377-390 - 3.
Tong SYC, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clinical Microbiology Reviews. 2015;28 (3):603-623 - 4.
Foster TJ. Antibiotic resistance in Staphylococcus aureus . Current status and future prospects. FEMS Microbiology Reviews. 2017;41 (3):43-49 - 5.
Zapotoczna M, O’Neill E, O’Gara JP. Untangling the diverse and redundant mechanisms of Staphylococcus aureus biofilm formation. PLoS Pathogens. 2016;12 (7):1-6 - 6.
Ribeiro M, Monteiro FJ, Ferraz MP. Infection of orthopedic implants with emphasis on bacterial adhesion process and techniques used in studying bacterial-material interactions. Biomatter. 2012; 2 (4):176-194 - 7.
Moormeier DE, Bayles KW. Staphylococcus aureus biofilm: A complex developmental organism. Molecular Microbiology. 2017;104 (3):365-376 - 8.
Krifa M, El Mekdad H, Bentouati N, Pizzi A, Ghedira K, Hammami M, et al. Immunomodulatory and anticancer effects of Pituranthos tortuosus essential oil. Tumor Biology. 2015;36 (7):5165-5170 - 9.
Puškárová A, Bučková M, Kraková L, Pangallo D, Kozics K. The antibacterial and antifungal activity of six essential oils and their cyto/genotoxicity to human HEL 12469 cells. Scientific Reports. 2017; 7 (1):1-11 - 10.
Swamy MK, Akhtar MS, Sinniah UR. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: An updated review. Evidence-based Complementary and Alternative Medicine. 2016; 2016 (1):1-21 - 11.
Myles IA, Datta SK. Staphylococcus aureus : An introduction. Seminars in Immunopathology. 2012;34 (2):181-184 - 12.
Lindsay JA. Genomic variation and evolution of Staphylococcus aureus . International Journal of Medical Microbiology. 2010;300 (2-3):98-103 - 13.
Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus . Lancet. 2001;357 (9264):1225-1240 - 14.
Alibayov B, Baba-Moussa L, Sina H, Zdeňková K, Demnerová K. Staphylococcus aureus mobile genetic elements. Molecular Biology Reports. 2014;41 (8):5005-5018 - 15.
Hodille E, Rose W, Diep BA, Goutelle S, Lina G, Dumitrescu O. Virulence in Staphylococcus aureus . Clinical Microbiology and Infection. 2017;30 (4):887-917 - 16.
Kim HK, Missiakas D, Schneewind O. Mouse models for infectious diseases caused by Staphylococcus aureus . Journal of Immunological Methods. 2014;410 :88-99 - 17.
Sakr A, Brégeon F, Mège JL, Rolain JM, Blin O. Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections. Frontiers in Microbiology. 2018;9 :1-15 - 18.
Ondusko DS, Nolt D. Staphylococcus aureus . Pediatrics in Review. 2018;39 (6):287-298 - 19.
Todd JK. Staphylococcal infections. Pediatrics in Review. 2005; 26 (12):444-450 - 20.
Tanwar J, Das S, Fatima Z, Hameed S. Multidrug resistance: An emerging crisis. Interdisciplinary Perspectives on Infectious Diseases. 2014; 2014 :1-7 - 21.
Agyeman PKA, Schlapbach LJ, Giannoni E, Stocker M, Posfay-Barbe KM, Heininger U, et al. Epidemiology of blood culture-proven bacterial sepsis in children in Switzerland: A population-based cohort study. Lancet Child & Adolescent Health. 2017; 1 (2):124-133 - 22.
Otto M. Community-associated MRSA: What makes them special? International Journal of Medical Microbiology. 2013; 303 (6-7):324-330 - 23.
Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus : Molecular characterization, evolution, and epidemiology. Clinical Microbiology Reviews. 2018;31 (4):1-103 - 24.
Chen CJ, Su LH, Chiu CH, Lin TY, Wong KS, Chen YY, et al. Clinical features and molecular characteristics of invasive community-acquired methicillin-resistant Staphylococcus aureus infections in Taiwanese children. Diagnostic Microbiology and Infectious Disease. 2007;59 (3):287-293 - 25.
Karakonstantis S, Kalemaki D. Evaluation and management of Staphylococcus aureus bacteriuria: An updated review. Infection. 2018;46 (3):293-301 - 26.
Marcó DPJ. Community-acquired Staphylococcus aureus , a recent problem. Archivos Argentinos de Pediatría. 2016;114 (6):500-502 - 27.
Chen M, Yu Q , Sun H. Novel strategies for the prevention and treatment of biofilm related infections. International Journal of Molecular Sciences. 2013; 14 (9):18488-18501 - 28.
Fisher RA, Gollan B, Helaine S. Persistent bacterial infections and persister cells. Nature Reviews. Microbiology. 2017; 15 (8):453-464 - 29.
Karauzum H, Datta SK. Adaptive immunity against Staphylococcus aureus . Current Topics in Microbiology and Immunology. 2017;409 :419-439 - 30.
Liu G. Molecular pathogenesis of Staphylococcus aureus infection George. Pediatric Research. 2010;65 (5):71-77 - 31.
Mirzaee M, Najar-Peerayeh S, Behmanesh M, Moghadam MF. Relationship between adhesin genes and biofilm formation in vancomycin-intermediate Staphylococcus aureus clinical isolates. Current Microbiology. 2015;70 (5):665-670 - 32.
Herman-Bausier P, Labate C, Towell AM, Derclaye S, Geoghegan JA, Dufrêne YF. Staphylococcus aureus clumping factor A is a force-sensitive molecular switch that activates bacterial adhesion. Proceedings of the National Academy of Sciences of the United States of America. 2018;115 (21):5564-5569 - 33.
Lacey KA, Geoghegan JA, McLoughlin RM. The role of Staphylococcus aureus virulence factors in skin infection and their potential as vaccine antigens. Pathogens. 2016;5 (1):1-17 - 34.
Campoccia D, Speziale P, Ravaioli S, Cangini I, Rindi S, Pirini V, et al. The presence of both bone sialoprotein-binding protein gene and collagen adhesin gene as a typical virulence trait of the major epidemic cluster in isolates from orthopedic implant infections. Biomaterials. 2009; 30 (34):6621-6628 - 35.
Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. Journal of Clinical Microbiology. 2003;41 (9):4465-4467 - 36.
Ghasemian A, Peerayeh SN, Bakhshi B, Mirzaee M. Detection of accessory gene regulator groups genes and cassette chromosome mec types among Staphylococcus aureus isolated from intensive care unit patients. Asian Pacific Journal of Tropical Disease. 2015;5 (2):153-157 - 37.
Pantosti A, Sanchini A, Monaco M. Mechanisms of antibiotic resistance in Staphylococcus aureus . Future Microbiology. 2007;2 (3):323-334 - 38.
Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nature Reviews. Microbiology. 2009;7 (9):629-641 - 39.
Hanssen AM, Ericson Sollid JU. SCCmec in staphylococci: Genes on the move. FEMS Immunology and Medical Microbiology. 2006; 46 (1):8-20 - 40.
Tiwari HK, Sen MR. Emergence of vancomycin resistant Staphylococcus aureus (VRSA) from a tertiary care hospital from northern part of India. BMC Infectious Diseases. 2006;6 (1):1-6 - 41.
Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, Flannagan SE, et al. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus . Science. 2003;302 (5650):1569-1571 - 42.
Santos AL, Santos DO, Freitas CC, Ferreira BLA, Afonso IF, Rodrigues CR, et al. Staphylococcus aureus : Visitando uma cepa de importância hospitalarStaphylococcus aureus : Visiting a strain of clinical importance. Jornal Brasileiro de Patologia e Medicina Laboratorial. 2007;43 (6):413-423 - 43.
Cázares-Domínguez V, Cruz-Córdova A, Ochoa SA, Escalona G, Arellano-Galindo J, Rodríguez-Leviz A, et al. Vancomycin tolerant, methicillin-resistant Staphylococcus aureus reveals the effects of vancomycin on cell wall thickening. PLoS ONE. 2015;10 (3):1-16 - 44.
Hall-Stoodley L, Stoodley P, Kathju S, Høiby N, Moser C, William Costerton J, et al. Towards diagnostic guidelines for biofilm-associated infections. FEMS Immunology and Medical Microbiology. 2012; 65 (2):127-145 - 45.
Yin W, Wang Y, Liu L, He J. Biofilms: The microbial “protective clothing” in extreme environments. International Journal of Molecular Sciences. 2019; 20 (14):1-18 - 46.
Flemming HC, Wingender J. The biofilm matrix. Nature Reviews. Microbiology. 2010; 8 (9):623-633 - 47.
Lebeaux D, Ghigo JM, Beloin C. Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiology and Molecular Biology Reviews. 2014; 78 (3):510-543 - 48.
Archer NK, Mark JM, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus biofilms properties, regulation and roles in human disease. Virulence. 2011;2 (5):445-459 - 49.
Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, et al. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. Journal of Bacteriology. 2007; 189 (11):4223-4233 - 50.
Khatoon Z, McTiernan CD, Suuronen EJ, Mah TF, Alarcon EI. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon. 2018; 4 (12):e01067 - 51.
Toole GO, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annual Reviews in Microbiology. 2000; 54 (1):49-79 - 52.
Heilmann C. Chapter 7 Adhesion mechanisms of staphylococci. Europe. Vol. 715(1). 2011. pp. 143-158 - 53.
Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster S, et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis andStaphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials. 2007;28 (9):1711-1720 - 54.
O’Gara JP. ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis andStaphylococcus aureus . FEMS Microbiology Letters. 2007;270 (2):179-188 - 55.
Marques VF, Motta CC, Soares BD, Melo DA, Coelho SM, Coelho ID, et al. Biofilm production and beta-lactamic resistance in Brazilian Staphylococcus aureus isolates from bovine mastitis. Brazilian Journal of Microbiology. 2017;48 (1):118-124 - 56.
Yap PSX, Yiap BC, Ping HC, Lim SHE. Essential oils, a new horizon in combating bacterial antibiotic resistance. Open Microbiology Journal. 2014; 8 (1):6-14 - 57.
Elshafie HS, Camele I. An overview of the biological effects of some mediterranean essential oils on human health. BioMed Research International. 2017; 2017 (1):1-14 - 58.
Sharifi-Rad J, Sureda A, Tenore GC, Daglia M, Sharifi-Rad M, Valussi M, et al. Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules. 2017; 22 (1):1-55 - 59.
O’bryan CA et al. Potential of plant essential oils and their components in animal agriculture—In vitro studies on antibacterial mode of action. Frontiers in Veterinary Science. 2015; 2 (35):1-8 - 60.
Barbosa L, Filomeno C, Teixeira R. Chemical variability and biological activities of Eucalyptus spp. essential oils. Molecules. 2016;21 (1671):1-33 - 61.
Raymond C, George N. Natural products chemistry: Sources, separations, and structures. Natural Products Chemistry. 2014; 1 :24-29 - 62.
Yang L, Wen KS, Ruan X, Zhao YX, Wei F, Wang Q . Response of plant secondary metabolites to environmental factors. Molecules. 2018; 23 (4):1-26 - 63.
Pazouli L, Niinenets Ü. Multi-substrate terpene synthases: Their occurrence and physiological significance. Frontiers in Plant Science. 2016; 7 (1019):1-16 - 64.
Dhifi W, Bellili S, Jazi S, Bahloul N, Mnif W. Essential oils’ chemical characterization and investigation of some biological activities: A critical review. Medicines. 2016; 3 (4):25 - 65.
Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils—A review. Food and Chemical Toxicology. 2008; 46 (2):446-475 - 66.
Jean-Michel M, Céline R. Natural Microbiol Agents. Vol. 8(1). Springer. 2018. p. 337 - 67.
Başer KHC, Demirci F. Essential oils. Kirk-Othmer Encyclopedia of Chemical Technology. 2000:1-37 - 68.
Chamorro ER, Zambón SN, Morales WG, Sequeira AF, Velasco GA. Study of the Chemical Composition of Essential Oils by Gas Chromatography. Vol. 1(1). Intech; 2012. pp. 307-324 - 69.
Wińska K, Mączka W, Łyczko J, Grabarczyk M, Czubaszek A, Szumny A. Essential oils as antimicrobial agents—Myth or real alternative? Molecules. 2019; 24 (11):1-21 - 70.
Tiwari BK, Valdramidis VP, O’Donnell CP, Muthukumarappan K, Bourke P, Cullen PJ. Application of natural antimicrobials for food preservation. Journal of Agricultural and Food Chemistry. 2009; 57 (14):5987-6000 - 71.
Nazzaro F, Fratianni F, De Martino L, Coppola R, De Feo V. Effect of essential oils on pathogenic bacteria. Pharmaceuticals. 2013; 6 (12):1451-1474 - 72.
Chimnoi N, Reuk-ngam N, Chuysinuan P, Khlaychan P, Khunnawutmanotham N, Chokchaichamnankit D, et al. Characterization of essential oil from Ocimum gratissimum leaves: Antibacterial and mode of action against selected gastroenteritis pathogens. Microbial Pathogenesis. 2018;118 :290-300 - 73.
Burt S. Essential oils: Their antibacterial properties and potential applications in foods—A review. International Journal of Food Microbiology. 2004; 94 (3):223-253 - 74.
Yap PSX, Yang SK, Lai KS, Lim SHE. Essential oils: The ultimate solution to antimicrobial resistance in Escherichia coli ? Pathogenesis and Biotechnological Applications. 2017;1 (2017):299-313 - 75.
Rai M, Paralikar P, Jogee P, Agarkar G, Ingle AP, Derita M, et al. Synergistic antimicrobial potential of essential oils in combination with nanoparticles: Emerging trends and future perspectives. International Journal of Pharmaceutics. 2017; 519 (1-2):67-78 - 76.
Lee K, Lee JH, Kim SI, Cho MH, Lee J. Anti-biofilm, anti-hemolysis, and anti-virulence activities of black pepper, cananga, myrrh oils, and nerolidol against Staphylococcus aureus . Applied Microbiology and Biotechnology. 2014;98 (22):9447-9457 - 77.
Rabin N, Zheng Y, Opoku-Temeng C, Du Y, Bonsu E, Sintim HO. Agents that inhibit bacterial biofilm formation. Future Medicinal Chemistry. 2015; 7 (5):647-671 - 78.
Vázquez-Sánchez D, Cabo ML, Rodríguez-Herrera JJ. Antimicrobial activity of essential oils against Staphylococcus aureus biofilms. Food Science and Technology International. 2015;21 (8):559-570 - 79.
Lopes-Lutz D, Alviano DS, Alviano CS, Kolodziejczyk PP. Screening of chemical composition, antimicrobial and antioxidant activities of Artemisia essential oils. Phytochemistry. 2008;69 (8):1732-1738 - 80.
Jafri H, Husain FM, Ahmad I. Antibacterial and antibiofilm activity of some essential oils and compounds against clinical strains of Staphylococcus aureus . Journal of Biomedical and Therapeutic Sciences. 2014;1 (1):65-71 - 81.
Pontes EKU, Melo HM, Nogueira JWA, Firmino NCS, Carvalho MG, Catunda Júnior FEA, et al. Antibiofilm activity of the essential oil of citronella ( Cymbopogon nardus ) and its major component, geraniol, on the bacterial biofilms ofStaphylococcus aureus . Food Science and Biotechnology. 2019;28 (3):633-639 - 82.
Tohidpour A, Sattari M, Omidbaigi R, Yadegar A, Nazemi J. Antibacterial effect of essential oils from two medicinal plants against Methicillin-resistant Staphylococcus aureus (MRSA). Phytomedicine. 2010;17 (2):142-145 - 83.
Porfírio EM, Melo HM, Pereira AMG, Cavalcante TTA, Gomes GA, De Carvalho MG, et al. In vitro antibacterial and antibiofilm activity of Lippia alba essential oil, citral, and carvone againstStaphylococcus aureus . Scientific World Journal. 2017;2017 (1):1-7 - 84.
Saeide S, Mahboubeh M, Javad RF, Fereshteh JMH. Antimicrobial and anti-biofilm effects of Mentha piperita andZataria multiflora on pathogenic bacteria. Journal of Medical Bacteriology. 2019;8 (5):1-7 - 85.
Kwieciński J, Eick S, Wójcik K. Effects of tea tree ( Melaleuca alternifolia ) oil onStaphylococcus aureus in biofilms and stationary growth phase. International Journal of Antimicrobial Agents. 2009;33 (4):343-347 - 86.
Aleksic V, Knezevic P. Antimicrobial and antioxidative activity of extracts and essential oils of Myrtus communis L. Microbiological Research. 2014;169 (4):240-254 - 87.
Melo RS, Azevedo AMA, Helena T, Rodrigues S, Ponte IL, et al. Effectiveness of Ocimum gratissimum L. essential oil against multidrug-resistant isolates ofStaphylococcus aureus andEscherichia coli . Molecules. 2019;24 (21):3864-3879 - 88.
Scandorieiro S, de Camargo LC, Lancheros CAC, Yamada-Ogatta SF, Nakamura CV, de Oliveira AG, et al. Synergistic and additive effect of oregano essential oil and biological silver nanoparticles against multidrug-resistant bacterial strains. Frontiers in Microbiology. 2016; 7 :1-14 - 89.
Lu M, Dai T, Murray CK, Wu MX. Bactericidal property of oregano oil against multidrug-resistant clinical isolates. Frontiers in Microbiology. 2018; 9 :1-14 - 90.
Walmiki MR, Ravishankar RV. Cell attachment inhibition and anti-biofilm activity of Syzygium aromaticum ,Cuminum cyminum andPiper nigrum essential oils against pathogenic bacteria. Journal of Essential Oil-Bearing Plants. 2017;20 (1):59-68 - 91.
Jardak M, Elloumi-Mseddi J, Aifa S, Mnif S. Chemical composition, anti-biofilm activity and potential cytotoxic effect on cancer cells of Rosmarinus officinalis L. essential oil from Tunisia. Lipids in Health and Disease. 2017;14 (1):1-10 - 92.
Sharifi A, Mohammadzadeh A, Zahraei Salehi T, Mahmoodi P. Antibacterial, antibiofilm and antiquorum sensing effects of Thymus daenensis andSatureja hortensis essential oils againstStaphylococcus aureus isolates. Journal of Applied Microbiology. 2018;124 (2):379-388 - 93.
Vitanza L, Maccelli A, Marazzato M, Scazzocchio F, Comanducci A, Fornarini S, et al. Satureja montana L. essential oil and its antimicrobial activity alone or in combination with gentamicin. Microbial Pathogenesis. 2019;126 :323-331 - 94.
Perez AP, Perez N, Lozano CMS, Altube MJ, de Farias MA, Portugal RV, et al. The anti MRSA biofilm activity of Thymus vulgaris essential oil in nanovesicles. Phytomedicine. 2019;57 :339-351 - 95.
Shahabi N, Tajik H, Moradi M, Forough M, Ezati P. Physical, antimicrobial and antibiofilm properties of Zataria multiflora Boiss essential oil nanoemulsion. International Journal of Food Science and Technology. 2017;52 (7):1645-1652 - 96.
Parrino B, Diana P, Cirrincione G, Cascioferro S. Bacterial biofilm inhibition in the development of effective anti-virulence strategy. Open Medicinal Chemistry Journal. 2018; 12 (1):84-87