Biotechnology Advances 26 (2008) 610617

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Biotechnology Advances
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b i o t e c h a d v

Research review paper

Non-thermal plasma technologies: New tools for bio-decontamination

M. Moreau a,b,c,, N. Orange a,b, M.G.J. Feuilloley a,b
a b c

Laboratory of Cold Microbiology, UPRES EA 2123, University of Rouen, Evreux, France Technological Platform of Evreux (GIP ITT), France GIE Comit Nord, Paris, France

a r t i c l e

i n f o

a b s t r a c t
Bacterial control and decontamination are crucial to industrial safety assessments. However, most recently developed materials are not compatible with standard heat sterilization treatments. Advanced oxidation processes, and particularly non-thermal plasmas, are emerging and promising technologies for sanitation because they are both efcient and cheap. The applications of non-thermal plasma to bacterial control remain poorly known for several reasons: this technique was not developed for biological applications and most of the literature is in the elds of physics and chemistry. Moreover, the diversity of the devices and complexity of the plasmas made any general evaluation of the potential of the technique difcult. Finally, no experimental equipment for non-thermal plasma sterilization is commercially available and reference articles for microbiologists are rare. The present review aims to give an overview of the principles of action and applications of plasma technologies in biodecontamination. 2008 Elsevier Inc. All rights reserved.

Article history: Received 7 April 2008 Received in revised form 31 July 2008 Accepted 3 August 2008 Available online 16 August 2008 Keywords: Non-thermal sterilisation Sanitation Bacterial resistance Advanced oxidation processes Gliding arc plasma

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Biological effects of plasmas . . . . . . . . . . . . . . . . . . 2.1. Denition of plasmas . . . . . . . . . . . . . . . . . . 2.2. Action of plasmas on the constituents of micro-organisms 3. Decontamination efciency of non-thermal plasmas . . . . . . 4. Plasma obtained at reduced pressure . . . . . . . . . . . . . 5. Plasmas obtained at atmospheric pressure . . . . . . . . . . . 5.1. Radio-frequency plasmas (RF) . . . . . . . . . . . . . . 5.2. Dielectric barrier discharges (DBD) plasmas . . . . . . . 5.3. Corona discharge plasmas . . . . . . . . . . . . . . . 5.4. Gliding arc discharge plasmas . . . . . . . . . . . . . 6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. 2. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 610 611 611 611 612 613 613 613 614 614 614 615 615

1. Introduction The development of bio-compatible polymers and the constraints of industrial safety have driven the emergence of new technologies of bio-decontamination. Most polymers are poorly resistant to heating

Corresponding author. Laboratory of cold microbiology, UPRES EA 2123, 55 rue Saint Germain, F-27000 Evreux, France. Tel.: +33 2 32 29 15 64; fax: +33 2 32 29 15 55. E-mail address: morgane.moreau@univ-rouen.fr (M. Moreau). 0734-9750/$ see front matter 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.biotechadv.2008.08.001

such that oven or autoclave sterilisation processes are generally inapplicable. Chemical treatments, such as ethylene oxide sterilisation, can be a solution but these techniques all suffer the drawback that traces of the active compound often remaining and constitute an unacceptable risk. Gamma irradiation is very effective but is poorly accepted by consumers, requires high security equipment and presents a problem similar to those of chemical treatment in that it generates large amounts of free radicals. Although less energetic, the use of electron beams (beta irradiation in other words) has very similar limitations. Purely physical techniques, such as high hydrostatic pressure, are chemically safer but require complex or expensive

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equipment and are generally incompatible with online treatments. Other techniques, such as microwaves, can be employed but are limited because they are non-thermal. Indeed, there is currently no perfect solution to sterilisation at ambient temperature. Techniques commonly designated as Advanced Oxidation Processes (AOP) have been emerging in this eld because without being totally devoid of defaults, they are essentially clean and generate only small amounts of persistent chemical species. These techniques are efcient with abatement levels up to 10 logarithms and are economically viable due to relatively low installation costs and energy consumption. The efciency of AOP is probably due to the fact that they combine both physical and chemical actions. These coupled techniques, involving for example ozone, hydrogen peroxide and UV radiation, generate in aqueous solutions very reactive oxidant components and free radicals including for example OHU, O, H2O2, and O3. 2 These techniques are recent, and rst appeared at the beginning of the 90's. They were initially developed for the sanitation of water and the destruction of environmental micro-organisms (Navarro et al., 2005; Shu and Chang, 2005). However, application to the destruction of pathogens has been also described (Liltved et al., 1993; Rodriguez Romo and Youssef, 2005). The most studied AOP is ozonation. The properties of O3 result from its oxidizing activity against organic matter. There are numerous applications of ozone in industry and it has been most widely employed for disinfecting water (Lezcano et al., 2000a,b; Mysore et al., 2004). The main limitation to ozone use is its cost when it is used at large scale and its toxicity if released into the immediate environment of operators. Since 1990, the use of ultrasound had been repeatedly proposed for the treatment of water (Phull et al., 1997; Mason et al., 2003; Stanley et al., 2004) and food (Mason et al., 1996). It is debatable whether ultrasound can be classied in the category of AOP. The mechanical energy of vibrations transferred to the liquid by ultrasound leads to a phenomenon of cavitation and its dissipation in the liquid phase breaks down H\OH bonds into reactive radicals. In addition to transient species, particularly OHU and HO2U, fairly stable chemical species including H2O2 are generated. These events are responsible for the strong oxidative potential of ultrasound (Henglein, 1987). Photocatalysis is another form of AOP which has been used for the purication of air (Hoang-Van et al., 1997; Jacoby et al., 1996), water (Maness et al.,1999; Herrera et al., 2000; Mendez-Hermida et al., 2007) and recently for the destruction of phytopathogens on plants (Yao et al., 2007). More recent than most of the other AOP, this technique is very promising. Pulsed-light is a method that involves the use of intense (N30,000 sunlight at sea level) and short (100300 s) pulses of photons in the solar spectrum. The technique probably acts due to the combination of UV, micro-metric scale thermic effects induced by electron excitation, and oxidative reactions resulting from free radical formation. It depends on the impact of photons that can be blocked by any non-transparent material pulsed-light is considered to be an ultra-surface technology (Elmnasser et al., 2007) although it can be applied to clear solutions (Feuilloley et al., 2006). Electric discharge and particularly non-thermal plasma constitute the last class of AOP and are the subject of this paper. These techniques have in common the formation of plasmas, i.e., mixtures of heavy (molecules, atoms, free radicals, ions) and light (electrons and photons) species generated by excitation of gas by electric discharges. The plasma gas can be directly cooled and projected onto the target or quenched by reaction with water. In both cases, highly reactive oxidative species are formed locally and can react with the macromolecules of contaminants. Here, we describe various non-thermal plasma techniques, their use for decontamination or sterilisation and their limitations. We consider the mechanisms that underlie micro-organism destruction and present some possibilities for the development of this technology.

2. Biological effects of plasmas 2.1. Denition of plasmas Plasma is dened as a neutral ionised gas. It is constituted by particles in permanent interaction; the particles include photons, electrons, positive and negative ions, atoms, free radicals and excited or non-excited molecules. Electrons and photons are usually designed as light species in contrast to the other constituents dened as heavy species. Consequently, the term plasma is considered to describe a state of matter in which the heavy species are neutral or ionised particles which result from an energetic transfer to a gas. Two categories of plasma, namely thermal and non-thermal can be dened according to the conditions in which they are created. The classication of plasma is based on the relative energetic levels of electrons and heavy species of the plasma. Thermal plasmas are obtained at high pressure (105 Pa) and need substantial power (up to 50 MW) to be observed. They are characterised by an almost local thermodynamic equilibrium between the electrons and the heavy species; the gas temperature is nearly the same for all the components of the plasma and can be very high (5 to 20 103 K). This type of plasma is found, for example, in plasma torches and in electric arcs. Non-thermal plasmas are obtained at lower pressures and use less power. They are characterised by an electron temperature much higher than that of the gas (macroscopic temperature) and consequently do not present a local thermodynamic equilibrium. Such plasma can be generated by electric discharges in lower pressure gases. A third category of plasmas, which limits are not clearly dened, has been proposed as intermediate between the two others. Usually, these plasmas are included in the category of the non-thermal plasmas because they are formed near atmospheric pressure and ambient temperature. These low temperature and medium pressure plasmas are of particular interest technically and industrially because they do not require extreme conditions. Typical illustrations of these plasmas are the corona discharge and the gliding arc discharge. 2.2. Action of plasmas on the constituents of micro-organisms The cytoplasmic membrane represents the boundary between the organised inner compartment of the cell and the environment. Consequently, it is the rst and often essential target for most of the chemical and/or physical techniques of decontamination. Either the structural integrity or specic functions of the cytoplasmic membrane can be targeted and affected. The action of chemical agents of decontamination has been extensively studied. Interestingly, in most cases their oxidising power is an essential element of their activity. Whether a compound is used for the treatment of water (Zanetti et al., 2003; Spratt et al., 2004), food (Rossini and Gaylarde, 2000) or pharmaceutical material (Mazzola et al., 2003), its efciency appears to correlate with its redox potential. These observations can easily be extrapolated to AOP that generate oxidising species in contact with the target. Three other mechanisms also contribute to the activity of chemical disinfectants: their electric charge which confers afnity for the micro-organism on the molecule, the constant of diffusion in the organism determining the number of active molecules available for the reactions and the pH (acidity) of the medium indirectly controlling oxidation. Very similar mechanisms are probably involved in the action of plasmas. In addition to very specic actions, plasma may have a general mechanical effect on the surface of the living organism. This effect is probably due to the abundance of OHU and NOU radicals in a plasma of humid air (Benstaali et al., 1998a,b; Laroussi and Leipold, 2004). Micro-organisms in plasma are exposed to an intense bombardment by these radicals probably provoking surface lesions that the living cell cannot repair sufciently quickly. This may explain why cells are in many cases destroyed very quickly. This process was termed etching

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by Pelletier (1993). It involves adsorption of the components of plasma onto the surface of micro-organisms to form volatile compounds that are then eliminated from the cells. Lerouge et al. (2000) compared micro-organisms to synthetic polymers formed essentially of C, H, N and O and suggested that etching may be responsible for the destruction of spores. The authors noted that the composition of the gas or mixture of gases used to generate the plasma, and thus responsible for free radical formation, determined the destructive efciency of the plasma against spores of Bacillus subtilis: viable spore counts fell by two log units with O2, O2/Ar, O2/H2, O2/Ar/H2, CO2 or O2/ CF4 and by ve log units with a mixture of O2 and CF4. Analogy between plasma and pulsed electric elds has been used for a detailed analysis of the action of plasma on the membranes. The phenomenon of electroporation provoked by pulsed electric elds on the cell membranes has been studied in detail (Pothakamury et al., 1995; Russel et al., 2000; Ulmer et al., 2002; Spilimbergo et al., 2003). It appears that plasma has very similar effects, inducing perforations in the membranes of micro-organisms (Sale and Hamilton, 1967; Castro et al., 1993; Pothakamury et al., 1995; Wouters and Smelt, 1997). Sato et al. (1996) identied chemical species (OHU and H2O2) created in water under the action of a high voltage electric eld. Remarkably, these species are the same as those formed in humid air plasma. Thus, the lesions to bacteria could be similar in these two cases. Ohshima et al. (1995) demonstrated that treatment of Saccharomyces cerevisiae with a pulsed electric eld causes the formation of pores that can be directly correlated to the intensity of the electric eld. Moreover, the destructive activity of the treatment against the micro-organism was linked to the number of the pores formed in the plasma membrane. In the case of electric elds, and by probable analogy with plasma, the formation of pores may be a consequence of a membrane compression phenomenon. Obviously, as observed in Salmonella typhimurium and Listeria monocytogenes, an increase in membrane permeability directly affects the transmembrane potential of the cells and their ability to regulate intracellular pH (Russel et al., 2000). This is particularly important because in addition to generating pores, humid air plasma provokes a marked acidication of the medium (Moreau et al., 2005, 2007). The fall of pH in the local environment can be partially explained by the formation of H3O+ ions in water due to electronic and ionic bombardment. Nitrogen oxides can also affect pH and conductivity through the formation of acids and ions in water (Burlica et al., 2002). However, micro-organisms including bacteria have a very dense cytoplasm and cytoplasmic proteins may efciently buffer the variations of pH. This would explain why in some species, for example Erwinia carotovora atroseptica, a decline in the pH of the medium is not an essential factor for bacterial inactivation (Moreau et al., 2007). Changes in the integrity of the membrane can directly affect DNA, particularly in bacteria where DNA is anchored to the membrane. Direct assays of total DNA extractible from bacteria after various times of exposure to a gliding arc plasma, show that this treatment substantially increases the release of DNA (Moreau et al., 2007); this may be due to a breakdown of the interactions between membrane proteins and the DNA (Moreau et al., 2007) and pore formation has been shown to be responsible for a leakage of DNA from the cell (Ohshima et al., 1995). This process is certainly increased by partial fragmentation of the DNA. (Oshima et al. 1995) showed that chromosomal, ribosomal and plasmid DNA in Escherichia coli is cleaved into small fragments when exposed to electrical discharges and that the efciency of the discharges depended on the initial conformation of the DNA (super-coiled DNA being more resistant than linear DNA). Partial hydrolysis of DNA has also been observed in strains of Erwinia exposed to gliding arc plasma (Moreau et al., 2007). The effect of plasma on DNA probably results from a combination of the activities of free radicals (NOU and OHU) and UV. The effects of UV on DNA are well known and include both the formation of thymine dimers and strand breaks. Indeed, the strong lethal effect of UV on micro-organisms and its effects on DNA are exploited by technique of

pulsed-light (Elmnasser et al., 2007). The action of plasmas may be similar to that of pulsed-light but the role of UV in plasma discharge decontamination is very controversial (Boudam et al., 2006) because the quantity of UV in plasma differs substantially according to the type of discharge employed and the gas used to create the discharge. For instance, few UV photons are emitted by a gliding arc discharge (Kuzmichev et al., 2000) but the plasma generated by this type of discharge nevertheless causes marked changes in the structure of DNA (Moreau et al., 2007). UV alone cannot explain the rapid and extensive destruction of bacteria by gliding arc plasma. For instance, Laroussi (1996) obtained complete destruction of a population of Pseudomonas aeruginosa in 10 min using gliding arc plasma whereas in the same conditions the effect of UV was very limited. This is consistent with the observations of Baier et al. (1992) who reported that UV emitted by a radio-frequency discharge is in itself not effective for micro-organism destruction. In plasma containing a low percentage of UV, it is probable that the effects on micro-organisms result from a combination of the actions of oxidative radicals and UV (Moreau et al., 2000). As shown with Bacillus subtilis spores (Moisan et al., 2001) UV photons probably partially destabilise and fragment DNA and spontaneous repair by the micro-organism may be rendered impossible by the rapid leakage of DNA through the pores resulting from the oxidative attack of the membrane by free radicals and the overall etching process. In the case of plasma generated by medium and low pressure discharges, with substantially greater generation of UV, the micro-organism may be killed mostly by DNA fragmentation by UV irradiation with erosion of the surface through photodesorption and etching completing the process. However, there is to take into account that the sterilizing efciency of UV depends on the wavelength of the radiation used. At atmospheric pressure, short-wavelengths vacuum UV are absorbed by air within some micrometers and thus rapidly loose their efcient for sterilisation (Fridman et al., 2007). In 2006, Boudam et al. wrote a review in which they focused particularly on the role of UV photons to explain bacterial death when they are submitted to a plasma treatment. Another possible, and less explored, target of plasma in living cells is proteins. Oxidative processes can affect enzymatic systems. In E. coli, Laroussi et al. (2001) observed metabolic changes, and in particular a decrease of the use of acid L-lactic acid and an increase of the use of the D-sorbitol, after plasma treatment. Various complementary biochemical assays have shown that plasma generated by gliding arc discharge increases the extraction yield of outer membrane proteins from Erwinia, presumably as a result of membrane destabilisation (Moreau et al., 2007). However, structural changes were also observed in outer membrane proteins with the disappearance of low molecular weight markers and a concomitant rise of proteins of high molecular weight. This observation may be a consequence of oxidative process, as suggested by Igumenov et al. (1988) in work with E. coli. Moreover, as indicated by the absence of changes to secreted enzymatic activity (Moreau et al., 2007) it appears that this effect of plasma may be specic to membrane-linked proteins, presumably because of their close interactions within the membrane. These observations tend to conrm that, as initially postulated, the membrane and/or surface of micro-organisms is the main target of plasma. 3. Decontamination efciency of non-thermal plasmas The rst tests of bio-decontamination by non-thermal plasmas were at the beginning of the 90's and the aim of these tests was to nd alternative technologies for the sterilisation of heat-sensitive materials (Baier et al., 1992; Grifths, 1993; Laroussi, 1996; Chau et al., 1996). The results appeared very promising, particularly in comparison with risky methods such as those employing toxic gas (Kolman et al., 2002). However, two key steps were required before industrial application of the process. The rst was the denition of the plasma itself and its operating conditions. The second concerned the resistance of the target (micro-organism) and the effect desired.

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The essential parameters linked to the plasma refer to the fact that different types of non-thermal plasma can be generated and their characteristics are noticeably different. The nature and proportions of the active species created in the discharge and thus the efciency of the treatment depends on the nature of the gas used to form the plasma (Boucher, 1985; Lerouge et al., 2000). The reactive species generated in the discharge also depend on the energy injected by the electric source. In the case of liquid targets, the physical and chemical properties of the solvent are important because it can evaporate during the treatment and then participate in the reactions. The composition and surface characteristics of the electrodes are also determinant because they guide the discharge and can evolve during the process. In particular, a layer of oxide can rapidly cover their surface, leading to the formation of a dielectric barrier that can modify the electrode potential and consequently the properties of the discharges. Finally, the efciency of the treatment depends on the distance between the electrodes, were the plasma is generated, and the target. Obviously, the greater the distance between the electrodes and the target, the less efcient the treatment. All these parameters have been studied using model systems involving Escherichia coli and Staphylococcus epidermidis and plasma generated by gliding arc discharges (Vitrac et al., 2000; Kamgang et al., 2007). The characteristics of the micro-organisms themselves are also important: even within a species or a single strain, the sensitivity to sanitation processes can differ, and an event as crucial as bacterial death remains very difcult to determine. For instance, bacteria are generally more resistant to destruction when in stationary phase than in exponential growth phase (Ponniah et al., 2003). A simple modication of culture medium can affect the sensitivity of a bacterium to a treatment. In some species, a single strain can be present as a vegetative form, generally sensitive to decontamination techniques, and as a sporulated form, often extremely resistant to chemical and physical agents. In some cases, particularly those involving heat-sensitive materials, these resistant forms cannot be destroyed (Nieburh and Dickson, 2003; Clerry-Barraud et al., 2004). Other bacterial species can generate viable but non-culturable forms (VNC). The exact nature of this state is still unclear (resistance form or sub-lethal evolution), and VNC remain very difcult to detect. An intrinsically difcult issue therefore is how to verify that the decontamination process is not itself inducing the formation of such VNC (Feuilloley et al., 2006). Moreover, the target may be bacteria in a planctonic form, but micro-organisms are much more frequently organised as biolms in which different physiological states co-exist, protected by an exopolymeric matrix such that they become very difcult to destroy (Mah and O'Toole, 2001; Stewart and Costerton, 2001; Wirtanen et al., 2001; Meyer, 2003). The nature of the surface beneath the biolm also contributes to microbial resistance (Briandet et al., 2003). In this review, we focus on plasmas that can be obtained at ambient temperature and atmospheric pressure and are therefore potentially the most applicable of these technologies. 4. Plasma obtained at reduced pressure This type of system is essentially represented by microwaves plasmas. A microwave emitter is inserted into the reactor in which the gas is conned. The antenna transmits energy to the gas that is then converted into plasma. The rst tests with this technique were at the beginning of the 80's (Boucher, 1980; Tensmeyer et al., 1981). Various gases have been used to generate plasma, including oxygen, (Nelson and Berger, 1989), N2O (Chau et al., 1996) and argon (Hury et al., 1998). A great diversity of micro-organisms has been tested for destruction, from the resistant spores of B. subtilis or B. stearothermophilus to the sensitive vegetative forms of E. coli (Chau et al., 1996; Hury et al., 1998). The inactivation of E. coli was investigated in detail by Purevdov et al. (2002) and Lee et al. (2005). In these studies, the duration of treatment was between 20 and

60 min. The most effective technique of direct destruction involved the use of plasma generated in a mixture of O2/CF4. In these conditions, a reduction of at least two log units of B. subtilis was obtained in less than 15 min (Lerouge et al., 2000). Another approach, spatial post-discharge, has also been studied. The plasma generated in argon, air or in a mixture of both, was projected onto a target at distance from its generation point. The value of this technique is that it can be used to sterilise complex structures as is usually necessary for the treatment of medical devices. B. subtilis spores were successfully inactivated (Moreau et al., 2000), but the treatment required was long (40 min) probably because the distance between the source and the target allows the short-lived reactive species of the plasma to dissipate. Moreover, as shown later by Moisan et al. (2002), the effect of microwave plasma requires synergy between UV and chemical components of the plasma. The highest efciency of post-discharge using microwaves plasmas was reported by Villger et al. (2004). In these experiments using N2/O2 plasma, a 13 log units reduction in the population of E. coli was obtained within 25 min. Recently, Pollack et al. (2008), developed a plasma sterilisation method using reduced pressure and microwaves discharges in order to sterilise the inner part of catheters which are very expensive and sensitive one use materials. 5. Plasmas obtained at atmospheric pressure Several techniques are able to generate plasmas at atmospheric pressure and with a macroscopic temperature close to ambient (Fridman et al., 2005). Such plasmas occur when a high potential difference is established between electrodes placed in a gas at atmospheric pressure. For that reason, they combine all electric, chemical, acoustic and photonic events occurring between the two conductors. In contrast with low pressure discharges, the plasmas generated in these conditions are heterogeneous and characterised by the streamers generated by local electron avalanches (discharges). Intense ionised zones are propagated in narrow bands where they strongly increase the electric eld. When a streamer connects the anode to the cathode, the ionised channel formed allows the discharge of the external circuit. If the power of the generator is sufcient, an electric arc is formed (Moussa, 1999). The general advantage of these techniques, besides the fact that they can be run at atmospheric pressure, is that they allow the formation of an abundance of active species and can be operated close to ambient temperature. The applications are multiple, including the treatment of surfaces, gases and aqueous solutions. Within the last decade of the discharges employed to create plasmas have been miniaturised and regrouped under the appellation of microplasmas. The aim of such technologies is to create plasmas as thin and small as possible that can be use for local treatments. For example E. Stoffels and her team developed a small-diameter lowpower radio-frequency atmospheric plasma or plasma needle in which a radio-frequency high voltage is applied to a single needle electrode located inside a concentric gas ow nozzle. This system derives from the so called microbeam plasma generator (Stoffels et al., 2002). Microplasmas are active on different bacterial species such as Streptococcus mutans (Goree et al., 2006) and Escherichia coli (Sladek and Stoffels, 2005) and the applications are multiple including microsurgery (Kieft et al., 2004) and dentistry (Perez-Martinez et al., 2007). The types and applications of microplasmas have been reviewed in details by Foest et al., in 2006. 5.1. Radio-frequency plasmas (RF) Radio-frequency discharges are obtained when the gas is subjected to an oscillating electromagnetic eld. The eld is generated by an induction coil surrounding the reactor (inductive discharge) or by separate electrodes arranged on the external surface of the reactor (capacitive discharge). These inductive or capacitive discharges have

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long been exploited for gas and surface treatments (Bellakhal et al., 1997a,b; Honda and Brandt, 1984). The rst proposal of an application of this technique to microorganism destruction resulted from the work of Menashi (1968) who developed a reactor in which a pulsed RF discharge generated argon plasma used to sterilise the inner surface of vials contaminated by bacterial spores. The authors reported a reduction in the spore count of 106 in less than 1 s. However, in this rst prototype the energy required to generate the plasma remained high and Peeples and Anderson (1985) suggested that this result was due to a mechanism of micro-incineration. Ashman and Menashi (1972),Boucher (1980) and Bithell (1982) developed other systems that allowed demonstration of the true sterilisation efcacy of RF plasmas in non-thermal conditions. Indeed, oxygen RF plasma was employed to sterilise objects sealed in packages (Bithell, 1982). To improve the use of RF plasmas, Boucher (1985) investigated the inuence of the gas and of the power of the discharge on the efciency of the treatment. He showed that CO2 RF plasma is more effective than argon RF plasma and that there is a direct correlation between the energy transmitted to the plasma and its destructive activity against micro-organisms. A two-step process was developed by Jacobs and Lin (1987). In this system, nowadays commercially available as STERRAD 100, H2O2 vapours are injected into a reactor in which a vacuum was created. RF discharges are generated in the second step, sterilizing the material present in the reactor. The effect of RF plasma can be rapid but is highly sensitive to the operating conditions. For instance, Nelson and Berger (1989) showed a 3.5 log unit reduction of B. subtilis counts by O2 RF plasma within less than 5 min; in another but very similar system, bacterial inactivation required 15 min (Fraser et al., 1976). More recently, Laroussi et al. used low frequency RF helium plasma and reported total sterilisation of Pseudomonas uorescens in 10 to 20 min (Laroussi, 1996) and a 4 log unit reduction of B. subtilis spore counts with 20 min (Laroussi et al., 2001). Soloshenko et al. (1999) achieved a reduction of 8 log units in B. subtilis counts in less than 2.5 min with luminescent discharges. As described above, the efciency of the treatment depended on the gas used and the power of the discharge (Soloshenko et al., 1999). Detailed analysis of the effect of RF plasmas suggested that short-lived reactive chemical species created in the discharges are responsible for the destruction of the micro-organisms whereas UV or local thermal effects may only play secondary or minor roles (Laroussi and Leipold, 2004). The efcacy of RF plasma is now well demonstrated. It can be used with sensitive material, such as of polyethylene terephtalate bottles (Koulik et al., 1999) and for the destruction of very resistant forms of micro-organisms including spores of Bacillus atrophaeus and Geobacterium stearothermophilus (Akitsu et al., 2005). Recent developments include applications to sterilizing medical devices and modifying the structure of polymers to prevent bacterial adhesion (Everaert et al., 1998; Youse Rad et al., 1998; Ben Gadri et al., 2000; Detomaso et al., 2003; Terajima and Koinuma, 2004). 5.2. Dielectric barrier discharges (DBD) plasmas DBD discharges are based on the use of a dielectric barrier in the discharge gap which stops electric currents and prevents the formation of sparks. DBD discharges, which are sometimes called silent discharges, usually operate at frequencies between 0.05 and 500 kHz. They have a large number of industrial applications because they operate at strongly non-equilibrium conditions at atmospheric pressure and reasonably high power levels, without using sophisticated pulsed power supplies (Fridman et al., 2005). They are applied for example, in ozone generation, CO2 lasers and as UV source in excimer lamps. This last decade, DBD found applications in biology and particularly for the destruction of bacteria or for medical applications. In 2006, Boudam et al., realised the destruction of spores

of B. subtilis with a DBD using a mixture of N2/N2O as the carrier gas. They obtained a reduction of more than 5 log units of spores within 10 min. Moreover they demonstrated that in this case, the role of gas and consequently the role of the quantity of UV photons emitted by the discharge are particularly important for the destruction of spores (Boudam et al., 2006). Staphylococcus, Streptococcus and yeasts (Candida), all isolated from human skin, were submitted to a treatment DBD. They were all completely destroyed in less than 15 s when exposed to the discharge (direct treatment) (Fridman et al., 2007). Recently Fridman et al. (2007) published a review in which they focussed on the non-thermal effects and mechanisms of interaction between plasma and living organisms. They particularly reported the development of the oating-electrode DBD (FE-DBD), which operates under conditions where one of the electrodes is a dielectric-protected powered electrode and the second a biological surface that can be human or animal skin or even an isolated organ. They showed that, when used in proper conditions, this type of device is devoid of negative effects on large size living targets and even stimulates tissue or skin regeneration. FE-DBD also allows accelerated blood coagulation, in addition to an efcient sterilizing action that makes it usable to treat non-living objects such as medical devices. 5.3. Corona discharge plasmas Corona discharge is the most extensively studied electric discharge plasma technique. The corona is a weakly luminous discharge, which usually appears at atmospheric pressure near sharp points edges or thin wires where the electric eld is sufciently large. Corona discharges can be ignited with a relatively high voltage, which mainly occupies the region around one electrode (Fridman et al., 2005). As it is very easy to operate, it has been tested for a multitude of applications from electroprecipitation to treatment of surfaces, liquids and aerosols (Chang et al., 1991; Bellakhal et al., 1997a,b). In 1997, Morar et al. reported the rst description of the effects of an air corona plasma on two parasites usually found on plants: Tetranicus urticae and Phorodum humuli. They noted that direct exposure to the discharge or incubation with air previously treated by the discharges, provoked different deleterious effects, including defective mobility, digestive dysfunction, dehydration and paralysis. In 80% of the cases, these alterations were lethal within 48 h. Lethality reached 99% after 72 h. The study of the bactericidal effect of the corona discharge was initiated by Kuzmichev et al. (2000). They compared the effect of various gases (air, O2, N2, and Ar) on B. stearothermophilus and obtained a reduction of 3 to 4 log units. They demonstrated that, as previously stated by Peyrous (1986) and Benstaali et al. (1998a), the presence of H2O in the gas substantially increases the efcacy of the process and suggested that OHU radicals are essential for bactericidal activity. This was conrmed by Yamamoto et al. (2001) who showed using E. coli that H2O2 exposed to a corona discharge was 1000 times more active than non-treated H2O2. As in the case of microwaves, this technique has been used for post-discharge treatments. Odic et al. (2002) reported a reduction of three log units in the viability of B. stearothermophilus. Reductions of 5 log units in 30 min have been reported for spores of the same species using the post-discharge of a plasma generated in an N2O2 gas mixture (Pointu et al., 2005). 5.4. Gliding arc discharge plasmas The principle of the gliding arc discharge was patented by Lesueur et al. in 1988 and was developed by Czernichowski et al. (Czernichowski et al., 2000; Czernichowski and Czernichowski, 2002). The reactor designed for the production of plasma by gliding arc discharges consists of two or more diverging metallic electrodes raised to a large potential difference (9 kV, 100 mA in open conditions). A gas (generally humid air) is injected into the gap between the electrodes. The arc that forms at the shorter inter-electrodes distance is blown and then

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jumps along the electrodes until it breaks into a plasma plume. A new arc immediately reforms for a new cycle. Unlike the corona discharges, this technique allows the use of high power and consequently leads to the formation of larger amounts of short-lived active species. Another advantage of this technique is that, although initially created for gas treatment (Czernichowski, 1994), it can be easily adapted for surface and even liquid treatments. The rst liquid targets tested were chemical pollutants (industrial wastes, organic components and solvents) present in water (Benstaali et al., 1998a,b; Fanmo et al., 2003; Moussa and Brisset, 2003; Abdelmalek et al., 2004). However, plasma generated by gliding arc discharges also rapidly showed potential for bacterial decontamination of liquids (Vitrac et al., 2000). The gliding discharge is well adapted to exploit very high electric power and thereby produce an abundance of reactive species. These chemical species, created both in and by the discharge, are responsible for a multitude of reactions when they are quenched in aqueous solutions (Hnatiuc, 2002). Because of the diversity of the molecules simultaneously present, plasma of humid air constitutes a very complex medium and, even nowadays, remains very difcult to model. It appears, however, that the properties of the gliding arc discharge can be deduced from those of the corona discharge (Moussa and Brisset, 1996; Benstaali et al., 1998a,b). Consequently, it is generally accepted that the model of corona discharge in humid air established by Peyrous (Peyrous, 1986, 1990) can be extrapolated to the gliding arc discharge. In view of the diversity of molecular species in humid air (N2, O2 and H2O), the plasma is formed by the decomposition of these elements under the electric eld and from the interactions between the newly created species (excitation, ionisation, dissociation, recombination). The result of all these interactions is a complex gas composed of electrons, atoms, molecules, photons, ions and notably excited species and radicals. The reactivity of free radicals and neutral species determines the quality of the plasma but minor species present can also have a large inuence by modulating the effects of neutral species (Moussa, 1999). The target itself (solid or liquid) is determinant for the oxidative, acidic and/or complexing properties of the plasma. A spectroscopic investigation of the gliding arc discharge in humid air revealed that the main species formed in the non-thermal phase are the radicals OHU and NOU (Benstaali et al., 1998a,b; Benstaali et al., 2002). More recently, it was shown that these radicals are found in the plume of the plasma (Delair, 2004). The radical OHU can act due to its electrophilic properties and x onto double bonds. The radical NOU mostly drives substitution reactions. The acid effects result from the presence in the discharge of NOU which, in contact with air, leads to the formation of NOx, and nitric and nitrous acids. When the plasma is projected onto a liquid target, it acidies the medium if it is not buffered. This acidifying effect, detectable with a corona discharge (Brisset et al., 1989), is substantially greater with a gliding arc discharge (Burlica et al., 2002; Moussa et al., 2005). The presence in the discharge of highly oxidative species, such as O and OHU, gives rise to the degradation of species exposed to the discharge. Depending on the operating conditions this can lead, ultimately, to a state of mineralization, with conversion of the organic materials into CO2 (Moussa and Brisset, 2003). The complexing effect is due to the presence of H2O2 in solution but also depends on the presence of catalysts, such as vanadium or titanium. Other than the work of Vitrac et al. (2000), studies on the bactericidal activity of the plasma generated by gliding arc discharges have been scarce until recently. It was rapidly obvious that the distance between the electrodes and the liquid target was a key parameter: the shorter the distance, the more rapid the bacterial inactivation. It also appeared that it was necessary to slow the gas ow to increase the residence time of the reactive species (Vitrac et al., 2000). Gliding arc discharge has now been applied to the destruction of various bacterial species. A reduction of six log units of a population of Staphylococcus epidermidis has been obtained in less than 1 min (Briandet et al., 2003).

It was particularly interesting to note that these bacteria showed poorer adhesion to material previously treated by gliding arc discharges suggesting the destruction of adhesion sites or the persistence of molecules with inhibitory activity. This technique also appeared very effective for the destruction of Hafnia alvei (KamgangYoubi et al., 2007) and various species of the former genus Erwinia including Erwinia carotovora atroseptica, Erwinia carotovora carotovora and Erwinia chrysanthemi (now Pectobacterium carotovorum atrosepticum, Pectobacterium carotovorum carotovorum and Dickeya chrysanthemi, respectively) (Moreau et al., 2005). Note that the action of gliding arc plasma against these species seemed to involve an etching mechanism, mainly affecting the outer bacterial membrane causing marked morphological changes, the release of constitutive proteins and the dissociation of membrane-linked DNA (Moreau et al., 2007). Work with Hafnia alvei revealed a temporal post-discharge mechanism which appears very promising because it suggests that the effect of the plasma can continue after the end of the treatment, and therefore without further energy consumption. Although outside the scope of the present review, it is important to note that this technique may be also very effective against viruses as suggested by a study with Inuenza A (Gallagher et al., 2005). The future of gliding arc discharge applications currently seems to centre on the treatment of liquids. Therefore, the possibility of directly immersing one or two electrodes in aqueous solution is being investigated (Hnatiuc, 2002). 6. Conclusion This review of the more recent applications of AOP, and particularly plasmas generated by electric discharges at ambient temperature for bacterial decontamination, illustrates both the broad diversity of technologies that can be deployed and also the remarkable efcacy of this process. Until very recently, most equipment composed experimental systems derived from apparatus built for other purposes, particularly the treatment of chemical pollutants. This has restricted comparisons between the different devices. Moreover, all the biological effects of plasma need to be rigorously characterised before accepting this technology as a valuable alternative to established approaches. With industrial partners, we have been developing the rst standardised glidarc treatment system for laboratory studies, allowing control of most of the essential parameters (electrode/target distance, gas ux, electrical power, temperature) and tight control of the bacterial population. This system will serve as a prototype for a more powerful device of industrial size that could be used for water decontamination in agriculture. Another aspect of the future of this technology is the possibility of coupling it with other decontamination processes such as intense pulsed-light and photocatalysis. Such associations are particularly promising for plasma-based technologies because they should allow tuning the system: a basal efcacy consuming little energy with the possibility of rapidly turning on high power as required by the degree of contamination. There are numerous potential applications for such devices, especially in view of the need for continuous and automated control of water distribution and recycling in towns and to supply industry.

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