Bacteria Inactivation via X-ray-Induced UVC ... - ACS Publications

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Bacteria Inactivation via X‑ray-Induced UVC Radioluminescence: Toward in Situ Biofouling Prevention in Membrane Modules Timothy A. Johnson, Elisa A. Rehak, Sushant P. Sahu, David A. Ladner, and Ezra L. Cates* Department of Environmental Engineering and Earth Sciences, Clemson University, Clemson, South Carolina 29634, United States S Supporting Information *

ABSTRACT: Germicidal UVC radiation is a highly effective, chemical-free tool for bacteria inactivation, but its application is limited to reactors and open areas that can accommodate lamps/LEDs and wiring. A relevant example of problematic bacterial colonization within UV-inaccessible confines where chemical techniques have found only limited success is biofouling of feed channels in high-pressure membrane elements for water treatment. Herein we demonstrate a unique method of generating UV internally using embedded radioluminescent (RL) particles excited by an external X-ray source. We further show that the magnitude of the emitted UV intensity and required X-ray dose rates are likely within effective and practical ranges for future application to antibiofouling technology. Assessment of three Pr3+-activated RL phosphor candidates revealed LaPO4:Pr3+ to have the most favorable luminescence properties, achieving over 2-log inactivation of E. coli in a thin water film with a 74 Gy dose of 150 kVp X-rays. The effect of UVC RL resulted in a doubling of inactivation rates over X-ray irradiation alone. Further efforts targeting membrane applications, which included X-ray penetration modeling, RO membrane UVC tolerance, and economic analysis, suggested that UVC RL shows promise for application to bacteria control in seawater RO.

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INTRODUCTION In the context of membrane processes for water treatment, biofouling refers to the establishment of bacterial biofilms and flocs within the membrane element feed channels. In high pressure membrane processes, this particular type of fouling is recognized as one of the greatest impediments to reducing operational and energy costs, having expensive consequences particularly for seawater and brackish water desalination (SWRO).1,2 During reverse osmosis (RO) and nanofiltration (NF), dissolved constituents, including potential nutrients, become concentrated at the membrane surface. For bacteria, the resulting environment is nearly ideal for growth of biofilms, which once formed are difficult to remove through typical cleaning cycles. Biofouling has many negative impacts on membrane systems, including flux reduction, increased pressure and energy requirements, and degradation of the membrane active layer by acidic microbial products.1,3−5 Combating bacterial colonization on multiple fronts is a continuous exercise in desalination plant operation. Due to the resistance of established biofilms to chemical and shear treatments, as well as the sensitivity of popular polymeric membrane materials to oxidative disinfectants, pretreatment is currently the most powerful tool for reducing biofouling in SWRO.6−8 Pretreatment operations may include solids removal processes, micro/ultrafiltration, as well as disinfection.9−11 With all strategies, however, any viable microorganisms that traverse the pretreatment train may infiltrate downstream membrane © XXXX American Chemical Society

elements, become immobilized therein, and proliferate. Periodic introduction of chemical biocides into membrane elements themselves is thus another important facet of biofouling control; however, the more effective hypochlorite disinfectants are damaging to polyamide membranes and are not viable options.8 Weaker oxidants such as chloramines are used in the absence of high bromide concentrations,12−15 while nonoxidizing biocides such as formaldehyde, glutaraldehyde, and quaternary ammonium compounds may also be employed.14 While UVC radiation is a more potent biocide and potentially less damaging to membranes than oxidants at effective doses, no practical method for producing UVC within the confines of spiral-wound RO modules has been demonstrated previously. Herein we propose a new method termed radioluminescence membrane biofouling control (RMBC). In theory, germicidal UVC radiation may be produced inside spiral-wound module feed channels by incorporating a chemically stable radioluminescent (RL) phosphor component, which is excited by Xrays delivered through the module from an external source. As shown in Figure 1, we envision the luminescent material as a coating or additive to the feed spacer, thus allowing emitted UV Received: August 21, 2016 Revised: October 9, 2016 Accepted: October 14, 2016

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DOI: 10.1021/acs.est.6b04239 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

luminescent decay times, many of which show emission in the UVC range.26−29 While inconsequential to scintillator applications, this latter quality is especially relevant to RMBC. Still, it is presently unknown whether the magnitude of UVC emission under X-ray excitation at practical dose rates is sufficient to inactivate bacteria rapidly. Figure 2 depicts the

Figure 1. Example layout of the radioluminescence membrane biofouling control (RMBC) concept, showing (A) an external X-ray source (e.g., a flat panel source22); (B) a spiral-wound membrane element; (C) a penetrating X-ray beam; and (D) a UVC-radioluminescent feed spacer achieving bacterial inactivation.

to radiate throughout the feed channel and inactivate microorganisms on the internal surfaces, as well as in the bulk feed solution. The theorized advantages of RMBC are numerous, including the following: reduced potential for membrane oxidative damage; the highly effective, broad spectrum biocidal action of UVC attributed to dimerization of the pyrimidine components of DNA; lack of chemical residuals in the concentrate solution; minimal modification to the spiral-wound membrane element configuration; and in situ, permanent bacteria killing ability without pausing membrane operation. This approach also contrasts with the many types of surface-functionalized antimicrobial membranes currently under study by many groups,16−19 in that deposition of dead bacteria or other foulants onto the membrane surface would not obscure the killing mechanism. Several studies have also demonstrated that UVC can penetrate biofilms to some extent, adding further robustness.20,21 Finally, the RMBC concept would allow full tunability of the radiation dosing regimen via electronic control of the X-ray source. Programmed on/off cycles and tube current/voltage could be easily optimized to achieve the most cost-effective technology with respect to electricity consumption. To enable bacteria inactivation by UVC inside spiral-wound membrane elements, two components are required: a radiation source that can penetrate water and polymer layers to deliver energy to within the module and a denser luminescent material that can intercept the radiation and downshift it to more potent germicidal wavelengths. X-rays or γ radiation of 102 keV or greater can achieve the first step, with X-rays being a more practical option with the widespread availability of compact sources. For context, typical diagnostic X-ray sources operate at accelerating voltages of 20−150 kV, thus producing broad spectrum Bremsstrahlung emission with upper photon energy limits of 20−150 keV.23 Sources for industrial nondestructive testing can produce more penetrating radiation, up to 600 keV.24 Radioluminescent materials have been reported extensively in the context of scintillation for radiation detection devices, comprising both lanthanide-doped dielectric scintillators and semiconductor materials in powder, ceramic, or single crystal form.25 Praseodymium-doped crystalline systems in particular have been studied due to their fast nanosecond-range

Figure 2. Mechanism of UVC radioluminescence by Pr3+-doped dielectric crystals. Photoelectric absorption of an X-ray photon initiates ionization events that build a population of conduction band electrons and valence band holes. The electrons and holes may recombine at Pr3+ centers to result in interconfigurational 4f5d → 4f emission.

general mechanism of UVC RL by Pr3+ ions in a wide-band gap matrix. Therein, photoelectric absorption of an X-ray photon produces an energetic, ionized free electron. Colliding with atoms in the material, the hot electron instigates cascading production of a population of additional ionized electrons. Ultimately, lower energy collisions result in excitation of valence band electrons into the crystal’s conduction band to build a population of electron−hole pairs; recombination of the pairs at Pr3+ centers results in emission of light.26 Due to the favorable energy position of the 4f5d band of Pr3+ in high crystal field strength environments, its 5d → 4f interconfigurational transitions are well-known to have energies in the UVC range for many host crystals.30,31 For the present work, a review of published literature revealed YPO4, LaPO4, and Lu2Si2O7 as promising hosts for Pr3+-activated antibacterial RL, due to their primary emission peaks within the germicidal range when doped with Pr3+, as well as their relatively high densities.32−34 Along with favorable optical properties such as high electron/ hole mobility and low occurrence of trapping defects, density (and high z composition) is important in maximizing X-ray absorption and achieving efficient excitation.25 The most effective approach for RMBC, we predict, is a high density RL material coupled with higher energy X-rays (≥100 keV). This combination would minimize background X-ray attenuation by water and polymers while still maintaining adequate absorption by the luminescent component. In this work, our goal was to dissect RMBC into its key phenomena and study these quantitatively through both experiments and basic simulations, in order to validate the concept and justify future research on antibiofouling efficacy. Also included is an assessment of some of the challenges we anticipate in developing RMBC technology. Experimental study of the potential for UVC damage to the membrane active layer and the predicted impact on membrane element operational lifetime were conducted. It is also interesting to consider safety B


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Characterization. RL spectra were obtained using a benchtop X-ray source for excitation (Amptek Mini-X) with electrode settings of 50 kV and 80 μA. Powder samples were packed into a sample holder facing a detection system and irradiated from a 45° angle. Emitted luminescence was collected by a UV grade fused silica focusing lens and directed through an optical chopper and into a detection monochromator. The detection system has been described previously.31 Following proper radiation safety protocol, the sample and source were contained within a Pb-lined shielding box that coupled to the detection monochromator and included electrical interlocks. X-ray diffraction (XRD) patterns of phosphor samples were obtained using a Rigaku Miniflex diffractometer (Cu kα radiation), and patterns were analyzed using PDXL2 or Jade software. SEM images were taken using a Hitachi S3400 variable pressure scanning electron microscope. UVC RL-induced Microbial Inactivation. In order to assess the feasibility of killing bacteria in close proximity to an emitting surface via X-ray induced UVC RL, experiments were performed using borosilicate glass Petri dishes with a thin layer of RL phosphor coated onto the bottom. Dishes were coated by making a slurry of the ethanol and phosphor material (2 g) that was swirled in an even layer on the bottom of the Petri dish and dried in an oven at 90 °C. The dishes were then heated in a muffle furnace at 700 °C for 30 min to lightly sinter the phosphor particles in place. Escherichia coli (ATCC 8739) stock suspensions in phosphate-buffered saline were prepared as in previous work35 with concentrations of 108 cfu/mL. For irradiation experiments, 3 mL of suspension was placed into the prepared Petri dishes and covered using a polystyrene lid to prevent contamination. This amount was just enough to cover the entire dish bottom in liquid. Suspensions were not diluted in order to more closely simulate high bacterial loading conditions in a membrane element feed channel. For each irradiation, one dish was placed in the beam path of a 300 kV (maximum) X-ray source (ICM D3006) housed in an X-ray cabinet and controlled by an external controller. Irradiations were conducted at various tube currents and accelerating voltages depending on the experiment. The source was air-cooled and resulted in some heat buildup within the cabinet, with the inside temperature reaching up to 38 °C as measured by a digital thermometer probe. After exposure, samples were serially diluted and assayed for viability using the spread plate method.36 All data points were performed in triplicate via separate experiments. Control experiments included use of uncoated glass Petri dishes containing E. coli to evaluate the inactivation resulting from X-rays alone and use of phosphorcoated dishes without X-ray exposure at 37 °C to detect any chemical toxicity effects, as well as undoped (nonluminescent) phosphor-coated dishes to account for X-ray scattering or catalytic effects by the material that were unrelated to inactivation by UVC RL. The dose rate of X-rays delivered by the source for various current and voltage settings was quantified in pre-experiments by irradiating personal film dosimeter badges for durations of a few seconds, set precisely by programming the source controller. The badges were placed in the same location as samples during E. coli experiments. The dose delivered to the badges was analyzed by a certified commercial lab using thermoluminescence (Mirion Technologies), and dose rates (Gy/min) were derived by dividing by the programmed exposure time. Doses delivered during microbial experiments

issues pertaining to radiation use, the capital cost of integrating X-ray sources and shielding into water treatment facilities, and the cost-benefit of RMBC for biofouling control. Supplementary discussions on these subjects are included in the Supporting Information. In short, we assert that safety can be easily addressed and that the economic outlook is promising but relies on the expansion of new flat panel X-ray source technology − a direction in which the industry is already moving.

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EXPERIMENTAL SECTION Materials. Orthophosphate samples were prepared from Y2O3 (99.9999%, Rare Earth Products), La(NO3)3·6H2O (99.999%, Alfa Aesar), and NH4H2PO4 (99.999% Acros Organics). 1.77 M Lutetium nitrate aqueous solutions were prepared from Lu2O3 (99.999%, Alfa Aesar) stock by boiling in 1:1 nitric acid at slight stoichiometric excess and diluting to the proper volume. Aqueous stock solutions of the Li+ (1 M) and Pr3+ (0.2 M) nitrates were prepared from LiNO3 (99.99%) and Pr(NO3)3·6H2O (99.99%) powders (Alfa Aesar). The LiNO3 crystalline powder (Alfa Aesar) was of unspecified hydration and was thus dried at 104 °C in air for several days prior to apportionment. Tetraethyl orthosilicate (TEOS, 99.999%, Sigma-Aldrich) served as the silicon source and gelling agent for the synthesis of Lu2Si2O7 samples. Powder Bi4Ge3O12 (BGO, 99.9995%) was purchased from Alfa Aesar, while a 10 × 10 mm polished BGO single crystal was purchased on eBay. Phosphor Synthesis. Lithium codoped LaPO4:Pr3+ and YPO4:Pr3+ phosphors were prepared by a solid state reaction with synthetic stoichiometries of (La or Y)1‑x‑yPrxLiyPO4‑y (though it is unknown whether charge compensation for Li+ substitution occurs through oxygen vacancies or interstitial doping). YPO4:Pr3+ synthesis involved mixing of Y2O3, NH4H2PO4, and dopant solutions at the above ratios, wetmilling with mortar and pestle and a small amount of ethanol, then drying, and transferring to alumina crucibles. LaPO4:Pr3+ was prepared similarly with La(NO3)3·6H2O as the La3+ source. Mixtures were heated in air using a muffle furnace at 1000 °C for 16 h. A series of samples with varying dopant concentrations were synthesized in order to optimize for RL intensity. Pr3+ concentrations were generally varied from 0 to 5 mol %, and Li+ concentrations were initially held at 10 mol %. After optimizing Pr3+ concentration to result in the most intense RL emission, the Li+ concentration was varied from 0 to 15 mol % while holding the Pr 3+ at the optimized concentration. Lu2Si2O7:Pr3+ (lutetium pyrosilicate, LPS:Pr3+) phosphors with an assumed stoichiometry of Lu2‑x‑yPrxLiySi2O7‑y were prepared using a sol−gel method similar to that reported previously.31 Solutions of Lu(NO3)3, Pr(NO3)3, and LiNO3 were mixed stoichiometrically and dried overnight in an oven to form a solid hydrated salt. Water and ethanol at a 3:1 ratio were then added to form a 2.25 M (lanthanide basis) solution. TEOS was added to provide a 60% excess stoichiometric Si content,31 and the solution was stirred for 10 min and placed into a drying oven for 1 h at 70 °C and 2 h at 104 °C until a yellow, translucent xerogel was formed. The xerogel was stored in a desiccator overnight to harden, then ground into a fine powder with mortar and pestle, and placed in alumina crucibles. This precursor was calcined and annealed in a muffle furnace at 1000 °C for 3 h. Pr3+ and Li+ dopant concentrations were optimized for RL emission similarly to orthophosphate materials. C


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microbial dose response data described below. Full simulation methods are described in the Supporting Information.

could thus be calculated by factoring in the durations therein, with the dose rates measured under the same settings. For attenuation experiments (described below) in which samples were placed slightly further from the source window, a correction was performed using RadPro software to account for the additional divergence of the beam. This correction took into account the window-to-sample distance of the experiment as well as the target-to-window distance of the X-ray tube. As a demonstration of X-ray penetration ability, E. coli inactivation was also assessed in the presence of a real crosssection of RO membrane element material (complete with water) that was placed in between the X-ray source and the sample. To create the cross-section, a lateral portion of a used 4 in. diameter RO membrane element was cut with a power saw. A 1 cm-thick section of material comprising membrane layers, feed spacers, and permeate spacers was extracted and cut into a circle such that it fit into a polystyrene Petri dish. The sample was placed in the dish, to which deionized water was added to fill in the air spaces. The dish was then covered with a polystyrene lid and sealed with silicone adhesive. Biodosimetry. The UVC dose response of the employed strain of E. coli was evaluated to generate a model with which to indirectly estimate the emitted UVC by the RL phosphors during X-ray experiments. Undiluted bacterial suspensions were placed in Petri dishes in the same fashion as with X-ray irradiations but were positioned under a UVC collimated beam apparatus equipped with a low pressure mercury lamp (λ = 254 nm). A series of samples were irradiated for various times at 740 μW/cm2, as measured by a radiometer with a germicidal detector head (Solar Light Co.). The lamp output was allowed to stabilize for 15 min prior to measuring the intensity or conducting irradiations. Samples were assayed for viability and plotted against applied UV dose. A delayed Chick-Watson model was then fit,37 allowing estimation of UVC dose exposure (254 nm-equivalent) based on an observed inactivation. Membrane UVC Irradiation. To assess the risk of photoinduced membrane degradation during RMBC, Hydranautics SWC5 polyamide RO membranes were irradiated with UVC from a low pressure mercury lamp (254 nm). Coupons were cut to fit a SEPA II membrane cell (GE Osmonics) and then placed into a plastic storage bag that had a square cut out of one side, over which a fused silica glass window was placed and sealed with silicone adhesive. This container allowed UVC irradiation of the membrane while keeping it submerged in a minimal amount of deionized water to prevent desiccation damage. The collimated beam apparatus was used to irradiate the coupons at 740 μW/cm2, while the samples were kept at room temperature using a small fan. Membranes were exposed in triplicate to a variety of doses, controlled by exposure time, before assessing for their salt rejection and flux capacity. The salt rejection of each exposed membrane was tested using a GE Osmonics salt rejection system described previously.38 Flux was measured by recording the mass of permeate over time. Pressure was maintained at 600 psi with crossflow velocity of 0.15 m/s. The RO system was operated until the salt rejection was determined to be stable. Computer Simulations. Basic numerical models for X-ray penetration and UVC inactivation within a defined virtual spiral wound membrane element were constructed using tabulated Xray attenuation data from the National Institute for Standards and Technology (NIST)39 and published data on RL material light yields,40 as well as experimental luminescence and

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RESULTS AND DISCUSSION Phosphor Development. Measured XRD patterns for the three phosphor candidates are shown in the Supporting Information (Figure S1). Patterns matched the anticipated tetragonal zircon structure for YPO4,41the monoclinic monazite structure for LaPO4,42 and the monoclinic thorveitite structure for LPS.43 SEM images of LaPO4:Pr3+ and YPO4:Pr3+are shown in Figure S2A and B, respectively, revealing aggregated heterodisperse crystallites ranging from 100−102 μm, typical of solid state reactions. Generally, micron-sized crystallites result in more efficient luminescence for lanthanide-doped phosphors, compared to nanocrystals.44 The morphology of the LPS:Pr3+ material was considerably different (Figure S2C and D), showing a microceramic structure with highly fused, uniform crystallites of ∼10 μm. All the materials chosen were highly stable mineral systems that are nonwater-reactive.45,46 Figure 3 shows the RL spectra of the phosphors under 50 kVp X-ray excitation, as well as that of BGO powder − a

Figure 3. Radioluminescence emission spectra of UVC phosphors and BGO powder reference under 50 kVp X-ray excitation at room temperature.

common semiconductor RL reference material with reported light yield of approximately 9000 photons per MeV absorbed.40 Activator concentration optimization data may be found in Figure S3, which confirmed 2 mol % Pr3+ as most effective. Luminescence by Pr3+ is susceptible to concentration quenching via cross-relaxation,47,48 as seen in the weaker luminescence at higher concentrations. Furthermore, lithium codoping is well-known to enhance the luminescence properties of oxide-based lanthanide phosphors due to numerous structural and kinetic effects during heating.31,49 Herein, Li+ resulted in roughly 2-fold RL enhancements for all three materials. The correlation between Li+ concentration and RL intensity (data not shown) was not as well-defined as in Pr3+ optimization; ultimately, optimized doping concentrations of D


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Table 1. Radioluminescence Performance of UVC Phosphors, Including Efficiency (Integrated Peak Area) Normalized to That of BGO, UVC-Range Light Yield, Bulk Crystal Density, and Selected X-ray Attenuation Coefficients (μ)a phosphor 3+

LaPO4:Pr YPO4:Pr3+ LPS:Pr3+

total efficiency vs BGO

est. UVC light yield (ph/MeV)

2.1 1.2 1.8

1.7 × 10 6.5 × 103 7.4 × 103

density (g/cm3) 56

4

5.07 4.2657 6.2343

μ, 50 keV (cm‑1)

μ, 300 keV (cm‑1)

44.2 12.5 22.8

0.81 0.50 1.47

The μ values were calculated by the weighting of the individual elemental μ/ρ values obtained from NIST against mass fraction,39 summing the full stoichiometry, and multiplying by phosphor density. a

YPO 4 :Pr 3+ (2 % )Li + (15 % ), LaPO4:Pr 3+ (2 % )Li + (10 % ), and LPS:Pr3+(1%)Li+(10%) were selected. The YPO4:Pr3+ and LaPO4:Pr3+ orthophosphates exhibited broad RL emission in the 220−280 nm range, ideal for microbial inactivation and consistent with 4f5d → 4f emission reported previously under vacuum UV excitation.42,50 Weaker emission peaks were observed in the 300−400 nm range and 440−500 nm range, attributed to intrinsic host emission from defects51−53 and intra4f Pr3+ transitions,30,54 respectively. The La3+ analog showed higher UVC RL intensity. Given its integrated UVC intensity of 1.8 (220−280 nm, 2.1 for total emission) normalized to that of BGO and the published BGO light yield of 9130 ph/MeV,40 the germicidal light yield of LaPO4:Pr3+ was estimated at 1.7 × 104 ph/MeV. (Under excitation by softer 50 kVp X-rays, it is reasonable to assume that all materials absorbed similar quantities of X-ray energy.) We further analyzed the RL emission of a single crystal BGO sample, which showed identical RL intensity to that of the powder material used herein (data not shown), adding further validity to the light yield estimate. Compared to the orthophosphate materials, LPS:Pr3+ showed lower-energy 4f5d → 4f UV emissions, typical of Pr3+ coordinated to SiO44− tetrahedra.31,55 Since a smaller fraction of its emission was in the UVC range, the estimated UVC light yield of this phosphor was somewhat lower, despite its comparable overall RL intensity. The UVC RL efficiencies of all the samples are summarized in Table 1. These results provide the first direct quantitative comparison of germicidal RL efficiency among several Pr3+-based materials. We note, however, that the above ranking is specific to the 50 kVp excitation used in our RL setup, under which all the samples were expected to show relatively strong X-ray attenuation. The results are thus only indicative of inherent RL quantum yield; for higher-energy X-ray excitation that is more penetrating, phosphor density and z-value is expected to play a larger role in overall RL performance, as crystals of lower density may not effectively absorb such an excitation beam. Published densities and calculated X-ray attenuation coefficients of the three candidates are given in Table 1. Accordingly, YPO4:Pr3+ was hypothesized to have lower relative RL intensity under higher-energy excitation (e.g., 300 keV) due to its lower μ at 300 keV. The higher μ for LPS:Pr3+ is also the reason for which it was chosen as a candidate, despite the less desirable spectral distribution of its emission. E. coli Inactivation by LaPO4:Pr3+ UVC RL. To provide the first known evaluation of biocidal activity by UVC RL phosphors, experiments were performed using a thin liquid layer of concentrated E. coli suspension over phosphor-coated Petri dishes covered with polystyrene lids. This setup crudely simulated bacteria within a hypothetical membrane module feed channel with RMBC, in that they were concentrated in close proximity to an RL-active surface. We focused on LaPO4:Pr3+ as a result of its RL showing the best balance of

intensity and germicidal emission spectrum (Figure 3). Figure 4a shows the inactivation that resulted from directing a 150

Figure 4. (a) E. coli inactivation dose response for LaPO4:Pr3+ RL and controls under 150 kVp X-ray irradiation. (b) E. coli inactivation by UVC RL phosphors and controls at various X-ray source accelerating voltages and dose of 30 Gy. Results for LPS:Pr3+ were impacted by chemical toxicity of the phosphor. All error bars depict standard deviations of three triplicate experiments.

kVp X-ray beam (1.23 Gy/min) through the covered dishes at various radiation doses. A dose of 74 Gy resulted in 2.1-log inactivation by the LaPO4:Pr3+ coating, attributed to a combination of UVC exposure from RL emission, as well as viability loss from X-ray exposure. With no RL coating, only 0.6-log inactivation occurred at the same dose, reflecting the lower biocidal action resulting from X-rays alone. Ionizing radiation is known to inactivate microorganisms primarily through DNA damage by water radiolysis products (H•, HO•, e−(aq), etc.).58 Control tests at 37 °C without irradiation for the same duration showed only 0.23 and 0.25-log inactivation with and without the LaPO4:Pr3+ coating, respectively, indicating no chemical toxicity. In a final control, undoped LaPO4 was used and resulted in 1-log inactivation at the same dose. Since LaPO4 is neither toxic nor UVC-luminescent, we believe the inactivation by undoped LaPO4 arose because the dense material intercepted and scattered X-rays that were otherwise transmitted in the uncoated dish experiment. In effect, the bacteria were exposed to a higher X-ray dose when LaPO4 was E


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Environmental Science & Technology present, and the same would be true for LaPO4:Pr3+. Thus, the net effect of UVC emission is seen by subtracting the inactivation by LaPO4 from that of LaPO4:Pr3+. UVC emitted by Pr3+ thus achieved more than a doubling of the inactivation rate compared to X-ray effects alone, and future improvements to phosphor RL efficiency would be directly additive. RL Phosphor Comparison. The RL spectroscopic analysis in Figure 3 showed that the three phosphor candidates each differ in emitted spectral distribution, as well as emission intensity under 50 kVp excitation. Both intensity and spectral overlap with bacterial DNA action spectra would affect antifouling activity in RMBC. Furthermore, as explained above, material density and elemental composition were hypothesized to have a greater importance in RL efficiency under irradiation by X-rays of higher energy than 50 kVp. Since the spectroscopy setup was limited to use of the smaller 50 kV benchtop source, comparison of RL emission spectra under high energy excitation by the 300 kV-max industrial source could not be completed; however, analysis of E. coli inactivation by the three materials under various X-ray energy regimes was conducted. These experiments provided a direct measure of antimicrobial action, as well as an indirect indication of RL efficiency at higher kVp. Figure 4b shows the bacteria inactivation following a dose of 30 Gy under three different voltage settings for the three phosphors and controls. The LaPO4:Pr3+ coating showed a significantly higher degree of inactivation compared to YPO4:Pr3+ for both 150 and 225 kVp irradiation. In fact, YPO4:Pr3+ resulted in the same inactivation, within error, as undoped YPO4 (data not shown) for all voltages used; thus, a biocidal enhancement by UVC-RL was not confirmed for this material, likely due to its lower UVC light yield and X-ray attenuation ability. At 300 kVp, inactivation by LaPO 4:Pr3+ was much lower, yet still significantly greater than the LaPO4 control. Contribution to biocidal action by UVC emission was thus evident at all accelerating voltages used with this material. The results for LPS:Pr3+ were starkly different from the other phosphors, with the three X-ray energy regimes showing no statistical difference in E. coli inactivation. Controls tests revealed, in fact, that the same degree of inactivation occurred with or without X-ray irradiation, indicating chemical toxicity upon exposing the bacteria to LPS. Weltje et al. reported that dissolved or complexed Lu3+ shows considerably higher toxicity to Vibrio f ischeri than other rare-earth ions, with an EC50 similar to Cu2+.59 We therefore speculate that E. coli inactivation herein mainly resulted from dissolution of Lu salt residues remaining from synthesis, rather than UVC-RL. A resulting ability to deter biofouling would likely be temporary, and the LPS:Pr3+ data are thus not illustrative with respect to RMBC. Biodosimetry. Figure S4 shows the UVC (254 nm) dose response curve of the E. coli employed in this work. The delayed Chick-Watson model revealed a rate constant of 0.122 mJ−1 (log10 basis), which describes much slower UV inactivation kinetics than previously published for this strain.35 This is most likely due to the high concentration of bacteria used −108 cfu/mL compared to the typical 105 used in UV studies − which resulted in visually noticeable turbidity. Bacteria in the bottom of the suspension were thus partially shielded from UV by other viable or nonviable bacteria, received a lower dose, and resulted in weaker apparent dose response. Using this model and the net inactivation due to UVC during the X-ray experiments (subtracting for inactivation due to X-

rays), the UV dose generated by 74 Gy X-ray dose was estimated at 14 mJ (254 nm equivalent). Attenuation Simulation Results. Construction and testing of a prototype RMBC-integrated spiral-wound RO module has been reserved for future research; nonetheless, results of our basic simulations presented below have provided insight into how such a system might perform. We considered a standard 8 in. diameter membrane element with a feed channelto-channel distance of 0.5 cm and LaPO4:Pr3+ incorporated into the channel of an amount equivalent to a 150 μm-thick solid layer. Figure 5a shows the calculated attenuation of

Figure 5. Simulation results for monochromatic X-ray beams of various photon energies passing through 8 in.-diameter spiral wound membrane elements, including (a) X-ray attenuation vs depth. Steep drops are due to attenuation by the dense phosphor layer; (b) predicted time required for 1-log inactivation of E. coli vs feed channel number (FC1 = outermost channel). Initial X-ray photon intensity of 9.9 × 1010 ph·cm−2·s−1 was derived from a 6.25 Gy/min dose rate by 150 keV photons.

monochromatic X-ray beams of various energies passing radially through the spiral layers. Such an analysis is limited, since emissions from actual X-ray sources comprise broad distributions of photon energies with varying penetration ability. For a source operating at 150 kV, only a minute fraction of emission will be near the 150 keV maximum energy, while the median photon energy emitted will be closer to half that value, depending on the tube target and window materials.23 Additionally, we did not factor in the pressure vessel housing material, which would add some degree of additional F


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Figure 6. (a) E. coli inactivation observed when a 1 cm-thick layer of RO element materials was used to attenuate the X-ray beam. LaPO4:Pr3+ was employed, with an X-ray dose of 60 Gy. (b) Effect of UVC (254 nm) exposure on salt rejection of polyamide RO membranes (Hydranautics SWC5).

attenuation, depending on the composition (i.e., PVC vs fiberreinforced plastic). Figure 5a predicts that a 50 keV beam would be ∼95% attenuated within the first 2 feed channels providing negligible potential for RMBC closer to the permeate collection tube. At 300 keV, however, the X-ray intensity is only diminished to 20% at the center. The steep drops in the data series are due to attenuation by the much denser phosphor layers and are less pronounced at higher photon energy. Thus, while the high-energy X-rays are more penetrating, they are also less effective at exciting the RL phosphor, as seen with the results of Petri dish experiments. To further illustrate, we employed the following parameters to predict the E. coli inactivation rate within each feed channel as a function of X-ray energy, serving as a surrogate for antibiofouling potential: (1) a designated “practical” X-ray dose rate of commercially available irradiators of 6.25 Gy/min (see the Supporting Information); (2) simulated data on X-ray intensity in each feed channel described above; (3) the predicted UVC light yield of LaPO4:Pr3+ based on spectroscopic comparison to BGO reference; and (4) the UVC dose response model of E. coli obtained herein (Figure S4). Figure 5b plots the predicted irradiation time required for 1-log bacterial inactivation in the range of feed channels in an 8 in. module as a function of applied monochromatic X-ray photon energy. It is seen that 50 keV is expected to result in fast inactivation within the first 5 feed channels (FCs) but quickly reaches impractical values deeper in the element. As expected, 300 keV resulted in the slowest inactivation at the module exterior but the fastest at the interior. With 150 keV photons, treatment times remained at under 30 min until FC11 but reached more impractical values at the module interior. Translation of the observed or calculated inactivation data herein into predicted RMBC efficacy is an ambiguous task, as there is no established quantitative relationship between inactivation rates of planktonic bacteria and long-term biofilm growth rates. Bak et al. found that bacteria inhabiting biofilms on used medical catheters required 100−1000 times the UVC dose to achieve disinfection-level inactivation compared to planktonic cells.21 However, this requirement only applies to well-established biofilms formed previously in the absence of a biocide − not for surface bacteria repeatedly exposed to UVC from the onset. Furthermore, prevention of biofouling does not require the feedwater or module surfaces to be disinfected; instead, only enough radiation damage to outcompete proliferation and/or discourage biofilm forming behavior would be required. In the evaluation of membrane photodamage presented below, we have assumed that significant inhibition of biofouling progression in an RO system could be

achieved by delivering a daily dose equal to that which resulted in 1-log E. coli inactivation in the experiments herein (approximately 30 Gy); however, this assumption is highly conjectural. During operation of RO systems, planktonic bacteria or bacteria recently adsorbed to relatively clean surfaces can be inactivated using mild chemical biocide treatments. The unique value of RMBC lies in its anticipated ability to inactivate “biofilm-ready” bacteria that may be protected by a small quantity of foulants or extracellular polymeric substances. The required treatment interval would thus depend on feedwater qualities and even the location of a specific membrane element within a membrane plant. Experimental Attenuation by Membrane Element Materials. As a simple demonstration of the ability of externally applied X-rays to activate RMBC through membrane materials, a 1 cm-thick radial section of an actual used RO element was employed as an attenuating medium. The medium was placed in between the X-ray source and the Petri dish containing E. coli and the LaPO4:Pr3+ phosphor layer. Figure 6a shows the inactivation resulting from a dose of 60 Gy applied with this configuration and using three different accelerating voltages. Interestingly, the choice of voltage (i.e., X-ray photon energy range) appears to have no effect on inactivation in this case. While higher energy X-ray photons result both in less effective radiolytic bacteria inactivation and UVC phosphor excitation, they will, however, more readily penetrate the attenuating medium sample. A balancing of these effects could explain the observed data and is generally consistent with our simulation results. The extent of inactivation for 150 kVp irradiation was approximately halved by the presence of the attenuating medium, based on the dose−response kinetics in Figure 4a. This result highlights the poor penetration ability of 150 kVp X-rays relative to the radial depth of a typical RO membrane element. For successful biofouling prevention, an Xray source that is either more powerful or more penetrating (or both) would be required, or development of more efficient RL materials may be pursued. Membrane Damage by Radiation. The final aspect of RMBC we evaluated was the potential for X-ray and UVC radiation to damage high pressure membranes under the doses in question. Successful prevention of biofouling that concurrently results in significant reduction in membrane operational lifetime is not an acceptable trade-off, and completing such an analysis at this stage is therefore essential to justifying additional research. Combernoux et al. have previously studied the dose tolerance of polyamide RO membranes to ionizing radiation and the associated radiolytic production of radical species.60 (Those authors were interested in the effects of γ G


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Environmental Science & Technology radiation emitted by radionuclides in certain feed solutions; nonetheless, the definition of dose equivalence units for ionizing radiation is such that 1 Gy of gamma photons has the same physicochemical effect on low density materials as 1 Gy of X-rays.) Their results indicated that no significant reduction in salt rejection occurs for doses of up to 0.1 MGy. Maintaining our assumed treatment dose of 30 Gy/d, this tolerance implies that polyamide membranes could endure RMBC for over 9 years − a highly promising result for RMBC feasibility. More detailed study under realistic desalination conditions is required to confirm these values, as is experimental determination of the required daily X-ray dose for biofouling prevention. The UVC dose tolerances of RO membranes have not been previously studied, thus we subjected membrane coupons to increasing UVC (254 nm) doses using a collimated beam apparatus and analyzed their salt rejection ability. Results for Hydranautics SWC5 polyamide membranes are shown in Figure 6b. Salt rejection remained statistically identical to control membranes, which were not irradiated, for doses up to 10,700 mJ. In Figure 4a, it is seen that the LaPO4:Pr3+ coating resulted in 1-log inactivation at the treatment dose of 30 Gy, with approximately half that value (0.5-log) resulting from emitted UVC when the results of the undoped LaPO4 control were subtracted out; and, according to the biodosimetry model, such a 0.5-log inactivation of the concentrated E. coli suspension will result from a UVC dose of 8.5 mJ. Comparing this dose value to that which resulted in critical salt leakage, we estimate that the salt rejection ability of the RO membrane may be compromised as a result of one treatment per day for 3.4 years. As with the ionizing radiation damage analysis above, these results are highly promising but are currently based on laboratory conditions and on many assumptions. UVC damage to polypropylene or other types of feed spacers should also be analyzed in the future, and it is presently unclear how concurrent X-ray and UVC irradiation would affect membrane damage. The effect therein may be additive, as the mechanisms of polymer damage for both types of radiation are primarily oxidative in nature.61,62 Finally, membrane water flux positively correlated with UVC dose (data not shown), consistent with the observed membrane damage and indicating no significant membrane densification that would impede RO. In conclusion, RL materials were used to inactivate bacteria though UVC emission for the first time, and the mechanism shows strong suitability for incorporation into SWRO for biofouling prevention. Future development of new and improved UVC-RL phosphors has the potential to drastically reduce X-ray dosing requirements, while system effectiveness when employing more intense, newly developed FPXSs should be included in future research. Our modeling work elucidated the behavior of X-ray attenuation and phosphor emissions in the context of spiral-wound membrane elements; however, more detailed methods that account for the broad-spectrum nature of X-ray source emissions are needed for precise performance analysis. Most importantly to engineering aspects, the quantitative relationship between biofilm growth rates and UVC dose rate should be formalized.

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Supplementary safety and cost-benefit discussion; modeling methods; XRD data; SEM micrographs; phosphor activator concentration optimization data; and E. coli UVC dose response data/model (PDF)

AUTHOR INFORMATION

Corresponding Author

*Phone: (864) 656-1540. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by an Early concept Grant for Exploratory Research (EAGER) from the U.S. National Science Foundation (CBET #1551534).

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REFERENCES

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.6b04239. H


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