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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 Comité 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 efﬁcient 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 ﬁelds 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 difﬁcult. 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. Deﬁnition of plasmas . . . . . . . . . . . . . . . . . . 2.2. Action of plasmas on the constituents of micro-organisms 3. Decontamination efﬁciency 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: firstname.lastname@example.org (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
Usually. It is debatable whether ultrasound can be classiﬁed in the category of AOP. 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. 2004). Non-thermal plasmas are obtained at lower pressures and use less power... and oxidative reactions resulting from free radical formation. mixtures of heavy (molecules.. highly reactive oxidative species are formed locally and can react with the macromolecules of contaminants. ions) and light (electrons and photons) species generated by excitation of gas by electric discharges. There are numerous applications of ozone in industry and it has been most widely employed for disinfecting water (Lezcano et al. Such plasma can be generated by electric discharges in lower pressure gases.. in plasma torches and in electric arcs. such as microwaves. Consequently. Here. The classiﬁcation of plasma is based on the relative energetic levels of electrons and heavy species of the plasma. 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... 2003. which limits are not clearly deﬁned. 2005). Typical illustrations of these plasmas are the corona discharge and the gliding arc discharge.000 × sunlight at sea level) and short (100–300 µs) pulses of photons in the solar spectrum. The plasma gas can be directly cooled and projected onto the target or quenched by reaction with water. The efﬁciency of AOP is probably due to the fact that they combine both physical and chemical actions. can be employed but are limited because they are non-thermal. Two categories of plasma. Deﬁnition of plasmas Plasma is deﬁned as a neutral ionised gas. 2004). Consequently. 2007). the use of ultrasound had been repeatedly proposed for the treatment of water (Phull et al. This type of plasma is found. 2004) and food (Mason et al. particularly OHU and HO2U. they are essentially “clean” and generate only small amounts of persistent chemical species. has been proposed as intermediate between the two others. This process was termed “etching” . More recent than most of the other AOP. 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. 2007) although it can be applied to clear solutions (Feuilloley et al. These observations can easily be extrapolated to AOP that generate oxidising species in contact with the target. Jacoby et al. water (Maness et al.. free radicals and excited or non-excited molecules. Thermal plasmas are obtained at high pressure (≥105 Pa) and need substantial power (up to 50 MW) to be observed. Moreau et al. Laroussi and Leipold. 1997. The most studied AOP is ozonation.. their use for decontamination or sterilisation and their limitations..1.. Mason et al. electrons. In addition to very speciﬁc actions. this technique is very promising. 2003. Indeed. These low temperature and medium pressure plasmas are of particular interest technically and industrially because they do not require extreme conditions. involving for example ozone. 2006). fairly stable chemical species including H2O2 are generated. The technique probably acts due to the combination of UV... hydrogen peroxide and UV radiation. The properties of O3 result from its oxidizing activity against organic matter. these plasmas are included in the category of the non-thermal plasmas because they are formed near atmospheric pressure and ambient temperature. They were initially developed for the sanitation of water and the destruction of environmental micro-organisms (Navarro et al. Stanley et al. for example. food (Rossini and Gaylarde. 1998a. and ﬁrst appeared at the beginning of the 90's.e. This may explain why cells are in many cases destroyed very quickly. Shu and Chang. generate in aqueous solutions very reactive oxidant components and free radicals including for example OHU. free radicals. These techniques have in common the formation of plasmas. micro-metric scale thermic effects induced by electron excitation. We consider the mechanisms that underlie micro-organism destruction and present some possibilities for the development of this technology. 2003).. Interestingly. Either the structural integrity or speciﬁc functions of the cytoplasmic membrane can be targeted and affected. and O3. namely thermal and non-thermal can be deﬁned according to the conditions in which they are created. / Biotechnology Advances 26 (2008) 610–617 611 equipment and are generally incompatible with online treatments.. i. Techniques commonly designated as Advanced Oxidation Processes (AOP) have been emerging in this ﬁeld because without being totally devoid of defaults. Rodriguez Romo and Youssef. 2005). These events are responsible for the strong oxidative potential of ultrasound (Henglein. 2 These techniques are recent.. 2. 1987).. 1996). 2000. These techniques are efﬁcient with abatement levels up to 10 logarithms and are economically viable due to relatively low installation costs and energy consumption. plasma may have a general mechanical effect on the surface of the living organism. In both cases. Micro-organisms in plasma are exposed to an intense bombardment by these radicals probably provoking surface lesions that the living cell cannot repair sufﬁciently quickly. we describe various non-thermal plasma techniques. atoms. This effect is probably due to the abundance of OHU and NOU radicals in a plasma of humid air (Benstaali et al. 1993. application to the destruction of pathogens has been also described (Liltved et al. 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. Whether a compound is used for the treatment of water (Zanetti et al.. However. Mysore et al.b. Electrons and photons are usually designed as “light” species in contrast to the other constituents deﬁned as “heavy” species. 2. 2000) or pharmaceutical material (Mazzola et al. The action of chemical agents of decontamination has been extensively studied. Herrera et al.. it is the ﬁrst and often essential target for most of the chemical and/or physical techniques of decontamination. Mendez-Hermida et al. 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. These coupled techniques. In addition to transient species.. atoms. 1997. Very similar mechanisms are probably involved in the action of plasmas.2. Biological effects of plasmas 2. A third category of plasmas. there is currently no perfect solution to sterilisation at ambient temperature.. Three other mechanisms also contribute to the activity of chemical disinfectants: their electric charge which confers afﬁnity for the micro-organism on the molecule. O−. They are characterised by an almost local thermodynamic equilibrium between the electrons and the heavy species.M. Spratt et al. its efﬁciency appears to correlate with its redox potential. positive and negative ions. Other techniques.b. 2005. Pulsed-light is a method that involves the use of intense (N30. in most cases their oxidising power is an essential element of their activity. 1996). 2007) and recently for the destruction of phytopathogens on plants (Yao et al. 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. the gas temperature is nearly the same for all the components of the plasma and can be very high (5 to 20 × 103 K). H2O2. the particles include photons.1999. Since 1990. Photocatalysis is another form of AOP which has been used for the puriﬁcation of air (Hoang-Van et al. Electric discharge and particularly non-thermal plasma constitute the last class of AOP and are the subject of this paper. 2004).. It is constituted by particles in permanent interaction. 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. 2000a.
after plasma treatment. humid air plasma provokes a marked acidiﬁcation of the medium (Moreau et al.. O2/Ar/H2. However. 2005. an increase in membrane permeability directly affects the transmembrane potential of the cells and their ability to regulate intracellular pH (Russel et al. the membrane and/or surface of micro-organisms is the main target of plasma. 2007). Indeed. (2000) compared micro-organisms to synthetic polymers formed essentially of C. micro-organisms including bacteria have a very dense cytoplasm and cytoplasmic proteins may efﬁciently buffer the variations of pH. 2007). 1995. the destructive activity of the treatment against the micro-organism was linked to the number of the pores formed in the plasma membrane.. Nitrogen oxides can also affect pH and conductivity through the formation of acids and ions in water (Burlica et al.... However. Pothakamury et al. 3. Spilimbergo et al.. 1995. Partial hydrolysis of DNA has also been observed in strains of Erwinia exposed to gliding arc plasma (Moreau et al. 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. (Oshima et al. 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.. 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. ribosomal and plasmid DNA in Escherichia coli is cleaved into small fragments when exposed to electrical discharges and that the efﬁciency of the discharges depended on the initial conformation of the DNA (super-coiled DNA being more resistant than linear DNA). These observations tend to conﬁrm that... and in particular a decrease of the use of acid L-lactic acid and an increase of the use of the D-sorbitol. two key steps were required before industrial application of the process. (1988) in work with E. Moreover. CO2 or O2/ CF4 and by ﬁve log units with a mixture of O2 and CF4.. The authors noted that the composition of the gas or mixture of gases used to generate the plasma. for example Erwinia carotovora atroseptica. Direct assays of total DNA extractible from bacteria after various times of exposure to a gliding arc plasma. In the case of electric ﬁelds. The effects of UV on DNA are well known and include both the formation of thymine dimers and strand breaks.. 1996). Oxidative processes can affect enzymatic systems. (1992) who reported that UV emitted by a radio-frequency discharge is in itself not effective for micro-organism destruction. few UV photons are emitted by a gliding arc discharge (Kuzmichev et al. 1992. there is to take into account that the sterilizing efﬁciency of UV depends on the wavelength of the radiation used. Lerouge et al. This would explain why in some species. As shown with Bacillus subtilis spores (Moisan et al. The results appeared very promising. In the case of plasma generated by medium and low pressure discharges. 1993. Moreover.. 2000). Decontamination efﬁciency of non-thermal plasmas The ﬁrst tests of bio-decontamination by non-thermal plasmas were at the beginning of the 90's and the aim of these tests was to ﬁnd alternative technologies for the sterilisation of heat-sensitive materials (Baier et al. 2007).. presumably because of their close interactions within the membrane. the lesions to bacteria could be similar in these two cases. 2007). (1996) identiﬁed chemical species (OHU and H2O2) created in water under the action of a high voltage electric ﬁeld. 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. 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. Grifﬁths. The second concerned the resistance of the target (micro-organism) and the effect desired.. Laroussi. For instance. The phenomenon of electroporation provoked by pulsed electric ﬁelds on the cell membranes has been studied in detail (Pothakamury et al. and by probable analogy with plasma. show that this treatment substantially increases the release of DNA (Moreau et al. Russel et al. This observation may be a consequence of oxidative process... 2007). Remarkably. N and O and suggested that “etching” may be responsible for the destruction of spores. and less explored. UV alone cannot explain the rapid and extensive destruction of bacteria by gliding arc plasma. 2000. 1996. 2007) it appears that this effect of plasma may be speciﬁc to membrane-linked proteins. 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. 1995) showed that chromosomal.. this may be due to a breakdown of the interactions between membrane proteins and the DNA (Moreau et al. particularly in comparison with risky methods such as those employing toxic gas (Kolman et al. inducing perforations in the membranes of micro-organisms (Sale and Hamilton. Castro et al. (2001) observed metabolic changes. In plasma containing a low percentage of UV. The ﬁrst was the deﬁnition of the plasma itself and its operating conditions. The effect of plasma on DNA probably results from a combination of the activities of free radicals (NOU and OHU) and UV.. 2002). Wouters and Smelt. a decline in the pH of the medium is not an essential factor for bacterial inactivation (Moreau et al. particularly in bacteria where DNA is anchored to the membrane. O2/Ar. Obviously.. Chau et al. For instance. Laroussi et al. Another possible. Various complementary biochemical assays have shown that plasma generated by gliding arc discharge increases the extraction yield of outer membrane proteins from Erwinia.. and thus responsible for free radical formation. 1997). target of plasma in living cells is proteins. 2007) and pore formation has been shown to be responsible for a leakage of DNA from the cell (Ohshima et al. the strong lethal effect of UV on micro-organisms and its effects on DNA are exploited by technique of pulsed-light (Elmnasser et al.. At atmospheric pressure. Moreau et al. as initially postulated. the formation of pores may be a consequence of a membrane compression phenomenon. Analogy between plasma and pulsed electric ﬁelds has been used for a detailed analysis of the action of plasma on the membranes. 1993.612 M. However. . as suggested by Igumenov et al. Sato et al. 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. Changes in the integrity of the membrane can directly affect DNA. Thus. This is consistent with the observations of Baier et al.. It appears that plasma has very similar effects. This process is certainly increased by partial fragmentation of the DNA. O2/H2. it is probable that the effects on micro-organisms result from a combination of the actions of oxidative radicals and UV (Moreau et al. 2007). 2007). coli. 1967. 2002). 2003). 2007). Boudam et al. / Biotechnology Advances 26 (2008) 610–617 by Pelletier (1993).. However. Ulmer et al. 2002. as observed in Salmonella typhimurium and Listeria monocytogenes. 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. In 2006. 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.. determined the destructive efﬁciency of the plasma against spores of Bacillus subtilis: viable spore counts fell by two log units with O2. short-wavelengths “vacuum” UV are absorbed by air within some micrometers and thus rapidly loose their efﬁcient for sterilisation (Fridman et al. This is particularly important because in addition to generating pores. these species are the same as those formed in humid air plasma. Ohshima et al. 2000). (1995) demonstrated that treatment of Saccharomyces cerevisiae with a pulsed electric ﬁeld causes the formation of pores that can be directly correlated to the intensity of the electric ﬁeld. 1995). H.. with substantially greater generation of UV. 2000) but the plasma generated by this type of discharge nevertheless causes marked changes in the structure of DNA (Moreau et al.. coli. presumably as a result of membrane destabilisation (Moreau et al. as indicated by the absence of changes to secreted enzymatic activity (Moreau et al. In E.
2000). an electric arc is formed (Moussa. air or in a mixture of both. 2006). A great diversity of micro-organisms has been tested for destruction. 2002). 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. the greater the distance between the electrodes and the target. For that reason. The antenna transmits energy to the gas that is then converted into plasma. The applications are multiple.. acoustic and photonic events occurring between the two conductors. was projected onto a target at distance from its generation point. The ﬁrst tests with this technique were at the beginning of the 80's (Boucher.. 2000).. coli was obtained within 25 min. When a streamer connects the anode to the cathode. the ionised channel formed allows the discharge of the external circuit. coli was investigated in detail by Purevdov et al. For example E. 2001. Wirtanen et al. 2000). a layer of oxide can rapidly cover their surface.. 4. B. Various gases have been used to generate plasma.1. The characteristics of the micro-organisms themselves are also important: even within a species or a single strain. Obviously. the effect of microwave plasma requires synergy between UV and chemical components of the plasma. The inactivation of E. Kamgang et al. often extremely resistant to chemical and physical agents. 2001. Recently. In particular. 2006) and Escherichia coli (Sladek and Stoffels. 2007). The highest efﬁciency of post-discharge using microwaves plasmas was reported by Villéger et al. 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. The nature and proportions of the active species created in the discharge and thus the efﬁciency of the treatment depends on the nature of the gas used to form the plasma (Boucher. The reactive species generated in the discharge also depend on the energy injected by the electric source.M. chemical. and as a sporulated form. subtilis was obtained in less than 15 min (Lerouge et al. from the resistant spores of B. A microwave emitter is inserted into the reactor in which the gas is conﬁned... subtilis or B. 2003). In these conditions. In some cases. (2004). 1985. The exact nature of this state is still unclear (resistance form or sub-lethal evolution). leading to the formation of a dielectric barrier that can modify the electrode potential and consequently the properties of the discharges. 5. 1980. the physical and chemical properties of the solvent are important because it can evaporate during the treatment and then participate in the reactions. Moreau et al. 2004) and dentistry (Perez-Martinez et al. bacteria are generally more resistant to destruction when in stationary phase than in exponential growth phase (Ponniah et al. they combine all electric. In some species. particularly those involving heat-sensitive materials.. In contrast with low pressure discharges. 1998). 2000. in 2006. stearothermophilus to the sensitive vegetative forms of E. (2002). spatial post-discharge. Moreover. Other bacterial species can generate viable but non-culturable forms (VNC). 1981).. we focus on plasmas that can be obtained at ambient temperature and atmospheric pressure and are therefore potentially the most applicable of these technologies. the sensitivity to sanitation processes can differ. These inductive or capacitive discharges have . these resistant forms cannot be destroyed (Nieburh and Dickson. 1999). In these studies. The ﬁeld 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). 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 ﬂow nozzle.. and an event as crucial as bacterial death remains very difﬁcult to determine. (Nelson and Berger. The most effective technique of direct destruction involved the use of plasma generated in a mixture of O2/CF4. Moreover. 2003). the plasmas generated in these conditions are heterogeneous and characterised by the streamers generated by local electron avalanches (discharges). Within the last decade of the discharges employed to create plasmas have been miniaturised and regrouped under the appellation of “microplasmas”. a reduction of at least two log units of B. 2004). the target may be bacteria in a planctonic form. Tensmeyer et al. Lerouge et al. is that they allow the formation of an abundance of active species and can be operated close to ambient temperature. 2005). and VNC remain very difﬁcult to detect. Hury et al. 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. 2001. For instance. The composition and surface characteristics of the electrodes are also determinant because they guide the discharge and can evolve during the process.. 5. the duration of treatment was between 20 and 60 min. were the plasma is generated. but micro-organisms are much more frequently organised as bioﬁlms in which different physiological states co-exist. Another approach. Such plasmas occur when a high potential difference is established between electrodes placed in a gas at atmospheric pressure. generally sensitive to decontamination techniques. (2005). 2005) and the applications are multiple including microsurgery (Kieft et al. Meyer. a 13 log units reduction in the population of E. including oxygen.. The plasma generated in argon. Finally. protected by an exopolymeric matrix such that they become very difﬁcult to destroy (Mah and O'Toole. a single strain can be present as a vegetative form. Stewart and Costerton. 1996) and argon (Hury et al. Plasma obtained at reduced pressure This type of system is essentially represented by microwaves plasmas. 1996.. (2002) and Lee et al. In the case of liquid targets.. gases and aqueous solutions.. and the target. 2003. 2003). 1998). the efﬁciency of the treatment depends on the distance between the electrodes.. (2008). subtilis spores were successfully inactivated (Moreau et al. besides the fact that they can be run at atmospheric pressure. Radio-frequency plasmas (RF) Radio-frequency discharges are obtained when the gas is subjected to an oscillating electromagnetic ﬁeld.. Microplasmas are active on different bacterial species such as Streptococcus mutans (Goree et al. coli (Chau et al. as shown later by Moisan et al. 1989). Intense ionised zones are propagated in narrow bands where they strongly increase the electric ﬁeld. In this review. 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.... The aim of such technologies is to create plasmas as “thin and small” as possible that can be use for local treatments. An intrinsically difﬁcult issue therefore is how to verify that the decontamination process is not itself inducing the formation of such VNC (Feuilloley et al.. the less efﬁcient the treatment. This system derives from the so called microbeam plasma generator (Stoffels et al. The types and applications of microplasmas have been reviewed in details by Foest et al. 2007). The general advantage of these techniques. 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. / Biotechnology Advances 26 (2008) 610–617 613 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. Clerry-Barraud et al. Pollack et al. including the treatment of surfaces. If the power of the generator is sufﬁcient. In these experiments using N2/O2 plasma.. N2O (Chau et al. has also been studied. The nature of the surface beneath the bioﬁlm also contributes to microbial resistance (Briandet et al. A simple modiﬁcation of culture medium can affect the sensitivity of a bacterium to a treatment.
Moreau et al. O2. the presence of H2O in the gas substantially increases the efﬁcacy of the process and suggested that OHU radicals are essential for bactericidal activity. In 80% of the cases. realised the destruction of spores of B. which mainly occupies the region around one electrode (Fridman et al. Corona discharge plasmas Corona discharge is the most extensively studied electric discharge plasma technique. this technique has been used for post-discharge treatments. DBD discharges. 2005). and Ar) on B.. Odic et al.. Staphylococcus. usually operate at frequencies between 0. in another but very similar system. (2007) published a review in which they focussed on the non-thermal effects and mechanisms of interaction between plasma and living organisms. To improve the use of RF plasmas. Honda and Brandt. 2000.2. 2005). As it is very easy to operate. FE-DBD also allows accelerated blood coagulation. 2004). / Biotechnology Advances 26 (2008) 610–617 long been exploited for gas and surface treatments (Bellakhal et al. bacterial inactivation required 15 min (Fraser et al.4.. 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. RF discharges are generated in the second step. H2O2 vapours are injected into a reactor in which a vacuum was created. subtilis with a DBD using a mixture of N2/N2O as the carrier gas. 1997a. this type of device is devoid of negative effects on large size living targets and even stimulates tissue or skin regeneration. such as of polyethylene terephtalate bottles (Koulik et al. Morar et al. 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 N2–O2 gas mixture (Pointu et al. CO2 lasers and as UV source in excimer lamps. 2003. (2002) reported a reduction of three log units in the viability of B. without using sophisticated pulsed power supplies (Fridman et al. Boucher (1985) investigated the inﬂuence of the gas and of the power of the discharge on the efﬁciency of the treatment.Boucher (1980) and Bithell (1982) developed other systems that allowed demonstration of the true sterilisation efﬁcacy of RF plasmas in non-thermal conditions. (2001) who showed using E. (1998a). Corona discharges can be ignited with a relatively high voltage. A two-step process was developed by Jacobs and Lin (1987). used low frequency RF helium plasma and reported total sterilisation of Pseudomonas ﬂuorescens in 10 to 20 min (Laroussi. which usually appears at atmospheric pressure near sharp points edges or thin wires where the electric ﬁeld is sufﬁciently large. They were all completely destroyed in less than 15 s when exposed to the discharge (direct treatment) (Fridman et al. stearothermophilus and obtained a reduction of 3 to 4 log units. including defective mobility.. As described above. coli that H2O2 exposed to a corona discharge was 1000 times more active than non-treated H2O2. stearothermophilus.b. 1998.. provoked different deleterious effects. in this ﬁrst 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. 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.. The arc that forms at the shorter inter-electrodes distance is blown and then . it has been tested for a multitude of applications from electroprecipitation to treatment of surfaces. They have a large number of industrial applications because they operate at strongly non-equilibrium conditions at atmospheric pressure and reasonably high power levels. (1999) achieved a reduction of 8 log units in B. 1997a.614 M. liquids and aerosols (Chang et al. Czernichowski and Czernichowski. in 1988 and was developed by Czernichowski et al. Bellakhal et al. 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. The effect of RF plasma can be rapid but is highly sensitive to the operating conditions. Recently Fridman et al. 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. The corona is a weakly luminous discharge. 2005). 1996) and a 4 log unit reduction of B. Moreover they demonstrated that in this case. However. Boudam et al.. Streptococcus and yeasts (Candida). Terajima and Koinuma.b). 1998. In this system. in addition to an efﬁcient sterilizing action that makes it usable to treat non-living objects such as medical devices. Ashman and Menashi (1972). Ben Gadri et al. 2000. in ozone generation. 2005).. More recently. Laroussi et al.. It can be used with sensitive material. The efﬁcacy of RF plasma is now well demonstrated. (Czernichowski et al.. 2001). reported the ﬁrst description of the effects of an air corona plasma on two parasites usually found on plants: Tetranicus urticae and Phorodum humuli. as previously stated by Peyrous (1986) and Benstaali 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. A gas (generally humid air) is injected into the gap between the electrodes. which are sometimes called silent discharges. This was conﬁrmed by Yamamoto et al. 5. digestive dysfunction. 1999). 2006). The study of the bactericidal effect of the corona discharge was initiated by Kuzmichev et al. They particularly reported the development of the ﬂoating-electrode DBD (FE-DBD). This last decade. subtilis counts in less than 2. these alterations were lethal within 48 h..05 and 500 kHz. The ﬁrst 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.5 log unit reduction of B.5 min with luminescent discharges. 2007). In 2006. They showed that. 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. 2004). They demonstrated that. nowadays commercially available as STERRAD 100®. 1982). oxygen RF plasma was employed to sterilise objects sealed in packages (Bithell. Youseﬁ Rad et al. 5. Nelson and Berger (1989) showed a 3.. Recent developments include applications to sterilizing medical devices and modifying the structure of polymers to prevent bacterial adhesion (Everaert et al. For instance. 100 mA in open conditions).3. 5.. Soloshenko et al. subtilis spore counts with 20 min (Laroussi et al... 1984). They obtained a reduction of more than 5 log units of spores within 10 min. Gliding arc discharge plasmas The principle of the gliding arc discharge was patented by Lesueur et al. subtilis counts by O2 RF plasma within less than 5 min.. were submitted to a treatment DBD. The authors reported a reduction in the spore count of 106 in less than 1 s. Indeed.. the efﬁciency of the treatment depended on the gas used and the power of the discharge (Soloshenko et al. Detomaso et al. 1991. N2. when used in proper conditions. 2002). They are applied for example. DBD found applications in biology and particularly for the destruction of bacteria or for medical applications. 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. In 1997.. They noted that direct exposure to the discharge or incubation with air previously treated by the discharges. (2000). Lethality reached 99% after 72 h. As in the case of microwaves. sterilizing the material present in the reactor. dehydration and paralysis. all isolated from human skin. They compared the effect of various gases (air. 1976).
2002. it acidiﬁes the medium if it is not buffered. with conversion of the organic materials into CO2 (Moussa and Brisset. Radiofrequency gas plasma (glow discharge). especially in view of the need for continuous and automated control of water distribution and recycling in towns and to supply industry. Unlike the corona discharges. Plasma chemical degradation of azo dyes by humid air plasma: yellow supranol 4 GL.. 2003. Fanmoé et al. allowing control of most of the essential parameters (electrode/target distance. 2005). molecules. 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 advantage of this technique is that. Brisset JL. It also appeared that it was necessary to slow the gas ﬂow to increase the residence time of the reactive species (Vitrac et al.. When the plasma is projected onto a liquid target. 2007) and various species of the former genus Erwinia including Erwinia carotovora atroseptica.b.. we have been developing the ﬁrst standardised glidarc treatment system for laboratory studies. are responsible for a multitude of reactions when they are quenched in aqueous solutions (Hnatiuc. the possibility of directly immersing one or two electrodes in aqueous solution is being investigated (Hnatiuc. 2003).. all the biological effects of plasma need to be rigorously characterised before accepting this technology as a valuable alternative to established approaches. remains very difﬁcult to model. organic components and solvents) present in water (Benstaali et al. 2007). 2004). 2004). dissociation. A reduction of six log units of a population of Staphylococcus epidermidis has been obtained in less than 1 min (Briandet et al. / Biotechnology Advances 26 (2008) 610–617 615 “jumps” along the electrodes until it breaks into a plasma plume. recombination). such as vanadium or titanium. Conclusion This review of the more recent applications of AOP. US Patent 3701628.. McGowan BD. 1994).. Moreau et al. 2005). plasma of humid air constitutes a very complex medium and. the plasma is formed by the decomposition of these elements under the electric ﬁeld and from the interactions between the newly created species (excitation. Cheron BG. Erwinia carotovora carotovora and Erwinia chrysanthemi (now Pectobacterium carotovorum atrosepticum. The complexing effect is due to the presence of H2O2 in solution but also depends on the presence of catalysts. Benstaali B.. Sorenson SE.. even nowadays. ions and — notably — excited species and radicals. Such associations are particularly promising for plasma-based technologies because they should allow tuning the system: a basal efﬁcacy consuming little energy with the possibility of rapidly turning on high power as required by the degree of contamination. 1998a. Moussa and Brisset. Ashman LE. 2003. This technique also appeared very effective for the destruction of Hafnia alvei (KamgangYoubi et al. Pectobacterium carotovorum carotovorum and Dickeya chrysanthemi. 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. atoms. detectable with a corona discharge (Brisset et al. The target itself (solid or liquid) is determinant for the oxidative. 1990) can be extrapolated to the gliding arc discharge. Gliding arc discharge has now been applied to the destruction of various bacterial species. however. Baier RE. and therefore without further energy consumption. The reactivity of free radicals and neutral species determines the “quality” of the plasma but minor species present can also have a large inﬂuence by modulating the effects of neutral species (Moussa. Moreover. Draou K. Because of the diversity of the molecules simultaneously present.193:29–34. mainly affecting the outer bacterial membrane causing marked morphological changes. Note that the action of gliding arc plasma against these species seemed to involve an etching mechanism. In view of the diversity of molecular species in humid air (N2. Akitsu T. most equipment composed experimental systems derived from apparatus built for other purposes. Moussa et al. to a state of mineralization. References Abdelmalek F. 2002). it can be easily adapted for surface and even liquid treatments. Abdelmalek et al. 1989). Depending on the operating conditions this can lead. O2 and H2O). The future of gliding arc discharge applications currently seems to centre on the treatment of liquids. illustrates both the broad diversity of technologies that can be deployed and also the remarkable efﬁcacy of this process..b. although initially created for gas treatment (Czernichowski. 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. (2000). Protective ﬁlms formed on copper by oxygen plasma treatment. particularly the treatment of chemical pollutants.18:236–42. 2005). and nitric and nitrous acids. plasma generated by gliding arc discharges also rapidly showed potential for bacterial decontamination of liquids (Vitrac et al. scarlet red nylosan F3 GL and industrial waste. Consequently... 1998a. Disinfection of dental operative instruments. is substantially greater with a gliding arc discharge (Burlica et al. leads to the formation of NOx. respectively) (Moreau et al. Benstaali et al. created both in and by the discharge. in contact with air. Surf Coat Technol 2005. A new arc immediately reforms for a new cycle. Kogoma M.. The radical NOU mostly drives substitution reactions. This acidifying effect. This has restricted comparisons between the different devices. Water Res 2004. Therefore.. Guarbi S. Other than the work of Vitrac et al. studies on the bactericidal activity of the plasma generated by gliding arc discharges have been scarce until recently. photons. However. 1996. gas ﬂux. 2002). including handpieces.b). It appears. There are numerous potential applications for such devices. Although outside the scope of the present review. J Oral Implantol 1992. More recently. 2000).. Meyer AE.. 1986. The acid effects result from the presence in the discharge of NOU which. gives rise to the degradation of species exposed to the discharge. Bellakhal N. (1972) Treatment of surfaces with low-pressure plasmas. Plasma sterilization using glow discharge at atmospheric pressure. 1998a. it was shown that these radicals are found in the plume of the plasma (Delair. 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. acidic and/or complexing properties of the plasma. ionisation. The presence in the discharge of highly oxidative species. Until very recently. Menashi WP. such as O and OHU.431:297–9. 2002). J Electroanal Chem 1997a. 6. Kasprzak SA. 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. . the release of constitutive proteins and the dissociation of membrane-linked DNA (Moreau et al.. ultimately. 1999). The result of all these interactions is a complex gas composed of electrons. Benstaali et al. electrical power. Ohkawa H. it is important to note that this technique may be also very effective against viruses as suggested by a study with Inﬂuenza A (Gallagher et al. The radical OHU can act due to its electrophilic properties and ﬁx onto double bonds. it is generally accepted that the model of corona discharge in humid air established by Peyrous (Peyrous. The ﬁrst liquid targets tested were chemical pollutants (industrial wastes.M. this technique allows the use of high power and consequently leads to the formation of larger amounts of short-lived active species. With industrial partners. The gliding discharge is well adapted to exploit very high electric power and thereby produce an abundance of reactive species. and particularly plasmas generated by electric discharges at ambient temperature for bacterial decontamination. Brisset JL. 2000). Addou A. the more rapid the bacterial inactivation. These chemical species. 2003). Tsuji M.38:2338–46. Kimura H. that the properties of the gliding arc discharge can be deduced from those of the corona discharge (Moussa and Brisset. Carter JM. It was rapidly obvious that the distance between the electrodes and the liquid target was a key parameter: the shorter the distance.
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