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Inactivation of Staphylococcus aureus in Water by a Cold, He/O2 Atmospheric Pressure Plasma Microjet
Na Bai, Peng Sun, Haixia Zhou, Haiyan Wu, Ruixue Wang, Fuxiang Liu, Weidong Zhu,* Jose L. Lopez, Jue Zhang,* Jing Fang
A direct-current, atmospheric pressure, cold plasma microjet (PMJ) sustained in a quasi-steady gas cavity in liquid was used to inactivate Staphylococcus aureus suspended in distilled water. While helium gas (with 2% O2 as additive) was used as working gas, an effective inactivation (>99%) was achieved in 6 min. The inactivation of bacteria was further veried by surface morphology examination and LIVE/ DEAD Baclight bacterial viability test (uorescence microscopy). The overall pH and temperature of the liquid were monitored during the plasma treatment and were found to be below the critical values for the survival of S. aureus. Hydroxyl radical (OH) was detected via electron spin resonance (ESR) spectroscopy, and alongside other intermediate reactive species, is attributed to the effective inactivation of S. aureus. End-on optical emission spectroscopy show strong atomic oxygen emission both in air and in water.
Introduction
Aqueous environment is susceptible to contamination by bacteria, protozoa, and viruses, which are in turn responN. Bai, H. Zhou, R. Wang, F. Liu, J. Zhang, J. Fang Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China E-mail: zhangjue@pku.edu.cn N. Bai, H. Zhou, F. Liu West China College of Stomatology, Sichuan University, Chengdu, China P. Sun, H. Wu, J. Zhang, J. Fang College of Engineering, Peking University, Beijing, China E-mail: zhangjue@pku.edu.cn W. Zhu, J. L. Lopez Department of Applied Science and Technology and Center for Microplasma Science and Technology, Saint Peters College, New Jersey, USA E-mail: wzhu@spc.edu
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sible for various illnesses such as kidney failure and degenerative heart disease. Some of them (such as Deinococcus radiodurans) can survive in rather extreme conditionsresistant to high heat and high dosage of UV radiation.[1,2] For large quantity water decontamination, such as in municipal water treatment plant, the common method is to add chemicals (such as chlorine) into water after a multi-stage ltration. This however involves transportation, storage, and proper disposal of residual of those chemicals as well as potential health issues. Ozone (O3), as a substitute of chlorine, started to gain popularity in recent years. Its high oxidation power, short lifetime and best of all, decomposition to O2 after the disinfection makes them ideal for water treatment. On a much smaller scale in the biomedical eld, one often deals with small volumes and low ow rates of liquids that contain very specic microbacterial contaminants, the bulky commercial ozone generators may not be appropriateneedless to say that some microbacterial contaminants in water are completely
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inert to ozone treatment. Ultra-violet light has recently been adopted for disinfection of water. New York City Department of Environmental Protection started to build the nations largest ultraviolet water treatment facility nearly 4 000 UV lamps are being installed in the facility. Discharges directly in and in contact with liquids may be another option. Intense UV radiation, shock waves, and reactive species generated in the process are believed to be effective agents to inactivate many forms of biological and chemical matters.[3] Sakiyama et al. achieved a 99.5% inactivation rate of Escherichia coli in 180 s by microplasma-initiated electrolysis in a normal saline solution.[4] Woedtke and coworkers observed a 7-log reduction of E. coli and Staphylococcus aureus (S. aureus) in a physiological saline solution (0.85%) following treatment of the solution by a surface dielectric barrier discharge (DBD).[5] In both cases, a small volume of liquid (tens to low hundreds of microliter) was used where the density of plasma (or power) registered on their treatment cell was probably huge. In this paper, we report the results of the inactivation of S. aureus suspended in a much bigger volume of distilled water (20 ml) by an atmospheric pressure, cold plasma microjet (PMJ). In contrary to our previous study (where compressed air was used as working gas),[6] pre-mixture of helium with 2% oxygen is used in this study. The inactivation of bacteria is evaluated via colony forming unit (CFU) count on Petri dish at different PMJ treatment time, and further veried by scanning electron microscope (SEM) and uorescent spectroscope. pH and temperature of the liquid system are monitored during the process. Electron spin resonance (ESR) spectroscopy and optical emission spectroscopy are used to study the active species in the plasma/liquid system.
Figure 1. Pictures of He/O2 PMJ sustained in(a) ambient air and (b) quasi-steady gas cavity in water.
water (the gas cavity and gas/liquid interface is not clearly shown in the picture due to the long exposure time). Staphylococcus aureus (Gram positive) was used as a model in the inactivation experiments. The bacteria, purchased from China General Microbiological Culture Collection Center (CGMCC number 1.2465), were cultured and reached the logarithmic growth phase. The suspension of bacteria was diluted to 104 CFU ml1 with nal volume 20 ml and the solution was subsequently treated with the He/O2 PMJ for 0, 2, 4, 6, 8, and 10 min, respectively. After plasma treatment, 150 ml of the suspension was spread on LB agar culture medium in a standard Petri dish (90 mm in diameter), which was incubated at 37 8C for about 21 h for CFU counts. The inactivation rate of bacteria is further calculated by the formula below:
Experimental Section
The plasma device used in this study comprised two copper tubes as electrodes separated by a ceramic tube. The device was driven by a direct current negative-polarity high-voltage power supply (Matsuada AU5R120) through a 5 kV ballast resistor. Detailed schematic diagram of the device as well as the electrical circuit can be found in ref.[7,8] Premixed helium and oxygen (volume ratio: 98% He and 2% O2, referred to He/O2 from here on) was used as the working gas at a ow rate of 2.5 slm. When sustained in air, the length of the He/ O2 plasma microjet does not resemble the long plume reported in the literatures,[911] probably mainly because of the activation mechanismDC power was used here instead of pulsed DC or rf power. Figure 1(a) shows a picture of the He/O2 PMJ sustained in air. Due to the low light emission from the PMJ, the picture was taken in a dark room with exposure time of about 3 s. The PMJ is %20 mm long at a sustaining voltage around 400 V, and an operating current of 35 mA. When immersed in water, the PMJ was sustained in a quasi-steady gas cavity with approximately the same sustaining voltage. Figure 1(b) shows a picture of the He/O2 PMJ sustained in
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ultra-pure water and used as the OH spin-trap reagent. Different solutions were exposed to the He/O2 plasma for a prescribed time. DMPO was added during the last minute to capture OH. Measurements of the DMPO-OH (spin-trapped adduct of OH) signals were carried out on an ESR spectrometer (E-500, Bruker Ltd, German) operating at room temperature. The ESR experiments were carried out under following conditions: central magnetic eld, 3 480.00 Gauss; sweep width, 100.0 Gauss; frequency, 9.768 GHz; modulation frequency, 100 kHz; power, 12.7 mW. The end-on light emission from the PMJ was collected through a quartz ber optics cable to the entrance slit of a 0.5 m spectrometer (SPEX Model 1870) equipped with a 1 200 groove mm1 grating. The dispersed emission spectra were recorded by an intensied CCD camera (Roper Scientic I-MAX-1024) in the exit plane of the spectrometer. A Roper Scientic ST-133 controller was used to control the data acquisition. When operated in air, the light was focused into one end of the ber optics cable via two convex lens. When the He/O2 PMJ was submerged in water, one end of the quartz ber optics cable was embedded at the bottom of the water container at a distance %5 mm away from the exit nozzle of the device.
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Figure 2. Inactivation rate of S. aureus treated with a He/O2 (2%) PMJ in water.
Colony forming units (CFUs) count and inactivation rate are used to demonstrate the inactivation of bacteria. The inactivation rate of S. aureus is dened as 100% minus the percent ratio of CFU counts of plasma treated sample to that of the control one. S. aureus in water was treated by He/O2 PMJ from 0 to 10 min and the inactivation rates are plotted in Figure 2 (solid square). A quick increase of inactivation rate from 0 to 99.6% was observed within the rst 6 min. The inactivation rate stayed around 99.8% thereafter. Colwell et al.[12] observed that pathogens in the environment may enter a viable but non-culturable state. To verify the inactivation of S. aureus in water by PMJ treatment, we evaluated the viability of the cells by monitoring the membrane integrity of the cells through uorescence microscopy. A mixture of SYTO 9 green uorescent nucleic acid stain and the red uorescent nucleic acid stain propidium iodide were used in this study. The stains differ in their ability to penetrate healthy bacterial cells. Live cells are stained green and dead cells Figure 3. Fluorescence microscopy images of S. aureus. S. aureus suspended in liquid was are stained red. The ratio of green to red treated with He/O2 (2%) PMJ for (a) 0 min, (b) 4 min, (c) 8 min, and (d) 16 min (live cells uorescence intensities provides a quanare stained green and dead cells are stained red).
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titative index of bacterial viability. For a clearer demonstration of the viability test under uorescence microscope, higher cell concentrations (108 CFU ml1) and longer PMJ treatment time was used during this test. As can be seen in Figure 3, bacterial cells were predominantly green for the control [Figure 3(a)] and for the sample treated for 4 min [Figure 3(b)]. However, majority of the cells in the sample treated for 8 min were stained red. An even clearer
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inactivation, the average liquid temperature, and acidity level were chosen as the main indices to evaluate the change of the properties of the liquid during the PMJ treatment. The temperature at the nozzle surface in the present case was measured to be around 77 8C in air at an operating current of 35 mA and a gas ow rate of 5 slm. However, when submersed in liquid, the continuous ow of roomtemperature gas, the mixing of the gas above the liquid surface, and the liquid itself serve as cooling agents in the system. The temperature of the liquid Figure 4. Scanning electron microscope (SEM) pictures of S. aureus (a) before and (b) after 10 min of He/O2 PMJ treatment in water. media increases with the PMJ treatment time and reaches equilibrium at %30 8C after 6 min of plasma exposure (Figure 5). This temperature is not sufcient for the inactivation of situation is seen in the sample treated for 16 min S. aureus in a liquid via purely thermal effects. [Figure 3(d)], indicating the death of the bacterial cells in the system. The pH value of the liquids was monitored with a microprocessor pH meter at different PMJ treatment time Scanning electron microscope pictures of S. aureus were and the results are also shown in Figure 5. PH value of the also taken before and after 10 min of PMJ treatment water decreased slightly from 7.4 to 6.2 during the 10 min (Figure 4). The bacteria underwent a transition from PMJ treatment. The slight change of the pH is possibly due initially smooth surfaces [Figure 4(a)] to severely deformed to the fact that during the experiments, the top of the surfaces [Figure 4(b)] after the PMJ treatment. Morphology treatment chamber was open. As a result, small amount of change of the cell wall is considered detrimental for the ambient air inevitably mixed into the liquid. Nitrogen and survival of the bacteria. This was not seen in the negative control samples where only He/O2 ow was introduced into oxygen from air interact with active species in PMJ (especially helium metastables) and form small amount the liquid. of nitric acid, therefore slightly acidied the water. Evaluation of Liquid Property The plasma-liquid system is a highly complex environment. The understanding of the system as well as the associated physical and chemical processes has been very limited. In an effort to further investigate the mechanism of S. aureus Evaluation of Hydroxyl Radical Hamaguchi and coworkers[13] showed in the treatment of E. coli in aqueous solution by a low-frequency helium plasma jet that a pH threshold was required for effective
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Figure 6. Electron spin resonance (ESR) spectrum of DMPO-OH signal in liquid treated with (a) He/O2 ow and (b) He/O2 PMJ.
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inactivation and attributed this to the fatty acid peroxidation by the perhydroxyl radical (HOO) rather than superoxide anion radical ( O ) directly. Similar results on the 2 inactivation of S. aureus have been reported in our previous work with an air plasma microjet.[6] In both cases, the pH value is required to be lower than a critical value (%4.7) for balance of the following reaction to be shifted to the left. HOO $ H O ! 2 (1)
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Although O is expected to exist in the liquid due to the 2 oxygen in the gas mixture, the slight decrease of pH to 6.2 is not sufcient to trigger the shift of the balance of the reaction. Hydroxyl radical (OH), with an oxidation potential of 2.8 V,[14] is most reactive and toxic among all reactive oxygen species (ROS). It tends to attack unsaturated fatty acids on cell membrane. Its presence can compromise the function of the membrane lipids and cause the transportation of ions and polar compounds into the cell,[1517] therefore inactivate the bacteria. However, this extreme reactivity also causes OH to be scavenged by virtually any organic molecule in its close vicinity, which accounts for its short life-span of about 109 s and its limited diffusion from the source.[18] Nevertheless, due to the continuous gas ow into the present system and the increased reaction surface in the quasi steady gas cavity created in water,[19] a considerable amount of bacteria are still exposed to OH directly. Therefore, it is meaningful to evaluate OH in the current system. ESR spectroscopy was used to detect OH produced in water by He/O2 PMJ. DMPO was used as the spin-trap reagent of OH, with DMPO-OH as the spin-trapped adduct (signal shows a 1:2:2:1 quartet pattern in the ESR spectrum[19]). Solution (as described in Experimental Part) treated with He/O2 gas ow was used as the control in this experiment. Figure 6 shows a comparison of relative DMPO-OH signals in liquids treated with He/O2 gas ow and with He/ O2 PMJ for 1 min, respectively. A strong DMPO-OH signal is observed for He/O2 PMJ case. The relative intensity of DMPO-OH signal at the same experimental conditions is even higher than that was observed in water containing 35% H2O2 treated by an air PMJ for the same amount of time.[20] To further evaluate the effect of OH on the inactivation of S. aureus, mannitol (0.3 mol l1) and glycerol (1.7 and 3.4 mol l1) were used as OH quenchers in the PMJ-water system. As expected, no OH adduct signal was observed in ESR spectrum (data not shown) when either mannitol or glycerol were added into the system. Neither was immediate inactivation of S. aureus observed. However, inactivation rate started to increase at longer PMJ exposure timehigher the concentration of hydroxyl quencher, later was the increase of inactivation rate observed (Figure 7). In
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Figure 7. Inactivation rate of S. aureus by He/O2(2%) PMJ in water with mannitol and glycerol as hydroxyl quencher.
one of the ESR experiments, water with mannitol or glycerol was treated by He/O2 PMJ for 5 min, with DMPO added around 4 min. Clear carbon oriented DMPO adduct signal was observed in the system (data not shown), indicating mannitol or glycerol was consumed in water by reacting with He/O2 PMJ generated reactive species and therefore alkoxyl radicals emerged. PH value was also recorded in this experiment and showed very little change in 10 min (from 7.3 to 7). Other ROS (such as O and 1O2) were also veried to exist 2 in the system via ESR spectroscopy, and are suspected to be either the precursors of OH or directly participate the inactivation of bacteria in water.[21] A few possible and important interactions among these ROS are: (i) O 2 can transform to H2O2 through self-dismutation: O2 e 2H ! H2O2, followed by homolysis of H2O2 to generate OH;[22] (ii) O can mediate the generation of 2 OH through HaberWeiss reaction: O H2O2 ! OH 2 OH O2;[23] (iii) 1O2 can be generated during the Haber Weiss reaction, the self-dismutation of O .[24] Hydrogen 2 peroxide concentration was evaluated with a H2O2 test kit (Model HYP-1; HACH Company, Loveland, Colorado, USA). The concentration of H2O2 in 20 ml distilled water treated with He/O2 plasma for 20 min was measured to be 4 6 mg l1. This is not a lethal value for the survival of S. aureus.[6] Optical Emission Spectroscopy Optical emission spectroscopy was used to investigate the active species generated in the He/O2 plasma. Figure 8 shows two different regions of the end-on optical emission spectra of He/O2 PMJ when operated in air at an operating current of 30 mA and a ow rate of 5 slm.
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Figure 8(a) shows the emission from 300 to 380 nm. Copper emissions at 319.4, 324.7, and 327.4 nm were observed due to the electrode material used in the device. Emissions at 337.1, 353.7, and 357.7 nm from N2 second positive system (C3PuB3Pg) were also clearly observed. This is due to the entrainment of air into the stream and excited by the long lived helium metastables (19.8 eV) via penning excitation.[25] Weak N emission at 391 nm was 2 also observed (data not shown). This is similar to what has been observed in DBD helium plasma driven by radio frequency power,[26,27] or pulsed DC power.[28] Figure 8(b) shows the emission from 440 to 850 nm. Major helium neutral emission lines observed when PMJ operated in air are from transition of 23P43D at 447.1 nm, 23P43S at 471.3 nm, 21P41D at 492.2 nm, 21S31P at 501.6 nm, 23P 33D at 587.6 nm, 21P31D at 667.8 nm, 23P33S at 706.6 nm, 21P31S at 728.1 nm (reference data taken from National Institute of Standards and Technology[29]).
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Strong atomic oxygen emission resulting from 35S35P at 777.2 nm was also observed in the spectrum. The emitting oxygen levels can be populated via a few channels: (i) direct electron impact excitation of O, O e ! O e; (ii) electron impact dissociative excitation of O2, O2 e ! O O e; (iii) dissociative attachment: O2 e ! O O; where dissociative excitation dominates the 777.2 nm oxygen line.[30] It is also possible that the impact of helium metastable atoms with oxygen molecule can dissociate O2 and populate the emitting oxygen level.[31] Very weak OH emission at 306309 nm was observed under the present condition. OH emission intensity, however, is related to the concentration of O2 in the gas mixture and is much stronger at lower oxygen concentrations. The results, together with the relative emission intensity of oxygen at 777.2 nm changing with the oxygen concentration in the gas mixture will be reported in a separate paper.
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When the He/O2 PMJ was submerged in water, collection of the light emission becomes much more challenging due to the interference of water and the lack of lens system. Nevertheless, helium and oxygen peaks observed in air still dominate the emission spectrum [Figure 8(c)]. As expected, in 300400 nm region, no N2 emission lines were observed due to the lack of air in the environment. Neither did we observe any Cu emissions. The emission at 656.3 nm is suspected to be a Ha line. However, no obvious OH emissions at 306309 nm were observed. We suspect that OH was seriously quenched in this water environment.[32] Weak emissions from NO-b system (2PX2P) and NO-g system (A2SX2P) as well as from copper were also observed in the 200305 nm region (data not shown). However, when submerged in water, these emissions will likely quench heavily and therefore their contribution to bacteria inactivation is not considered important. Although excessive amount of helium exist in the system with certain percentage in the high energy metastable states, its direct effect on the inactivation of bacteria is doubtful. Neither is the reaction of helium metastable with water considered effective in producing reactive species for the inactivation of bacteria. In another study, pure helium PMJ was used in water instead of He/O2 PMJ, where no inactivation was observed, indicating the major killing agent comes from ROS. Atomic oxygen is a strong oxidative species. However, to the best of our knowledge, there is very little research done on the direct effect of atomic oxygen on bacteria inactivation in water. Excited atomic oxygen has a life time of %30 ns.[33] We suspect that atomic oxygen can directly oxidize bacteria within its close vicinity or react with water molecule rst, generating intermediate species such as hydroxyl or hydrogen peroxide for the inactivation of bacteria. It is also worth noting that trace amount of ozone (a few ppm), was detected in air with an ozone analyzer.[21] When submerged in water, ozone can live for 1 000 s in room temperature[34] and is believed to interact with water rst to produce OH, therefore indirectly participate in the inactivation of bacteria.
cavity inside water. Compared to other approaches, the approach described here employs a simply setup, direct current and He/O2 gas mixture as working gas, and does not require the presence of electrolyte in water for the ignition and sustaining of the plasma.
Acknowledgements: The rst two authors contributed equally to this work. This research is sponsored by Bioelectrics Inc. (USA), National Basic Research Program (No. 2007CB935602) and MST Program of International Science and Technology Cooperation (under Grant # 2009DFB30370: Cold Plasma induced biological effect and its clinical application studies). The development of the PMJ device was funded in part by the Electro-Energetic Physics Program of the U.S. Air Force Ofce of Scientic Research (AFOSR) under grant number FA9550-08-1-0332. The Acknowledgment is also made to the Donors of the American Chemical Society Petroleum Research Fund for partial support of this research. The authors like to thank Huizhan Zhang from Peking University for her help with SEM, Jiawu Nian from the College of Engineering, Peking University, for his help with Fluorescence microscopy, and Lingxuan Wang from Key Laboratory of Photochemistry, Institute of Chemistry, Chinese Academy of Sciences for her technical support in ESR. The authors would like to thank Dr. Kurt Becker for his helpful discussions. One of the authors (W. Z.) would like to acknowledge Electro-Energetic Physics Program of the U.S. Air Force Ofce of Scientic Research (AFOSR) for their support for fundamental studies of the plasma jet under grant number FA9550-08-1-0332.
Received: June 11, 2010; Revised: December 29, 2010; Accepted: January 13, 2011; DOI: 10.1002/ppap.201000078 Keywords: atmospheric pressure; inactivation; oxygen species; plasma microjet
Conclusion
In conclusion, we demonstrated the effective inactivation (>99%) of S. aureus in distilled water in 6 min by a DC atmospheric-pressure cold He/O2 (2%) plasma microjet. PH value of the water changed from 7.4 to 6.2 while the overall water temperature reached %30 8C in a 10 min treatment neither of which reached a lethal value for the survival of bacteria. The inactivation is mainly attributed to hydroxyl radical generated in water by He/O2 plasma. The existence of hydroxyl radicals in the system was veried via ESR spectroscopy. Hydroxyl radicals could be generated via ROS (such as O , 1O2, O, and O3) with water molecule in the gas 2
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[6]
[7] [8]
K. Harada, S. Oda, Agric. Biol. Chem. 1988, 52, 2391. J. R. Battista, Annu. Rev. Microbiol. 1997, 51, 203. P. Bruggeman, C. Leys, J. Phys. D: Appl. Phys. 2009, 42, 05300. Y. Sakiyama, T. Tomai, M. Miyano, D. B. Graves, Appl. Phys. Lett. 2009, 94, 161501. K. Oehmigen, M. Hahnel, R. Brandenburg, Ch. Wilke, K. D. Weltmann, Th. von Woedtke, Plasma Process. Polym. 2010, 7, 250. F. Liu, P. Sun, N. Bai, Y. Tian, H. Zhou, Sh. Wei, Y. Zhou, J. Zhang, W. Zhu, K. Becker, J. Fang, Plasma Process. Polym. 2010, 7, 231. H. Feng, P. Sun, Y. Chai, G. Tong, J. Zhang, W. Zhu, J. Fang, IEEE Trans. Plasma Sci. 2009, 37, 121. J. F. Kolb, A. A. H. Mohamed, R. O. Price, R. J. Swanson, A. Bowman, R. L. Chiavarini, M. Stacey, K. H. Schoenbach, Appl. Phys. Lett. 2008, 92, 241501. M. Laroussi, X. Lu, Appl. Phys. Lett. 2005, 87, 113902. X. Lu, Z. Jiang, Q. Xiong, Z. Tang, X. Hu, Y. Pan, Appl. Phys. Lett. 2008, 92, 081502. J. L. Walsh, J. J. Shi, M. G. Kong, Appl. Phys. Lett. 2006, 88, 171501. R. R. Colwell, P. R. Brayton, D. J. Grimes, D. B. Roszak, S. A. Huq, L. M. Palmer, Nat. Biotechnol. 1985, 3, 817.
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[13] S. Ikawa, K. Kitano, S. Hamaguchi, Plasma Process. Polym. 2009, 7, 33. [14] R. Venkatadri, Robert. W. Peters, Hazard. Waste Hazard. Mater. 1993, 10, 107. [15] I. Fridovitch, Annu. Rev. Biochem. 1995, 64, 97. [16] M. Laroussi, F. Leipold, Int. J. Mass Spectrom. 2004, 233, 81. [17] B. H. J. Bielski, R. L. Arudi, M. W. Sutherland, J. Biol. Chem. 1983, 258, 4759. [18] J. Aikens, J. Biol. Chem. 1991, 266, 15091. [19] J. R. Harbour, V. Chow, J. R. Bolton, Can. J. Chem. 1974, 52, 3549. [20] P. Sun, J. Pan, Y. Tian, N. Bai, H. Wu, L. Wang, C. Yu, F. Liu, S. Wei, Y. Zhou, J. Zhang, W. Zhu, K. Becker, J. Fang, IEEE Trans. Plasma Sci. 2010, 38, 1892. [21] P. Sun, H. Wu, N. Bai, H. Zhou, R. Wang, H. Feng, F. Liu, W. Zhu, J. Zhang, J. Fang, Plasma Process. Polym. in review. [22] B. Halliwell, J. M. C. Gutteridge, Biochem. J. 1984, 219, 1. [23] Willem. H. Koppenol, Redox Rep. 2001, 6, 229. [24] A. U. Khan, Proc. Natl. Acad. Sci 1994, 91, 12365. [25] V. Leveille, S. Coulombe, Plasma Process. Polym. 2006, 3, 587.
[26] Jianjun. J. Shi, Dawei. W. Liu, Michael. G. Kong, IEEE Trans. Plasma Sci. 2007, 35, 137. [27] V. Leveille, S. Coulombe, Plasma Sources Sci. Technol. 2005, 14, 467. [28] X. Lu, Z. Jiang, Q. Xiong, Z. Tang, Y. Pan, Appl. Phys. Lett. 2008, 92, 151504. [29] Yu. Ralchenko, A. E. Kramida, J. Reader, and NIST ASD Team 2008. NIST Atomic Spectra Database (version 3.1.5), [Online]. Available: http://physics.nist.gov/asd3 2009, November 29. National Institute of Standards and Technology, Gaithersburg, MD. [30] R. E. Walkup, J. Chem. Phys. 1986, 84, 2668. [31] S. Wang, V. Schulz-von der Gathen, H. F. Dobele, Appl. Phys. Lett. 2003, 83, 3272. [32] P. Bruggeman, F. Iza, P. Guns, D. Lauwers, M. G. Kong, Y. A. Gonzalvo, C. Leys, D. C. Schram, Plasma Sources Sci. Technol. 2010, 19, 015016. [33] S. Reuter, K. Niemi, V. Schulz-von der Gathen, H. F. Dobele, Plasma Sources Sci. Technol. 2009, 18, 015006. [34] W. H. Glaze, Joon-Wun Kang, Douglas H. Chapin, Ozone: Sci. Eng. 1987, 9, 335.
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