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PII: S0043-1354(16)30130-0
DOI: 10.1016/j.watres.2016.03.003
Reference: WR 11887
Please cite this article as: Song, K., Mohseni, M., Taghipour, F., Application of ultraviolet light-
emitting diodes (UV-LEDs) for water disinfection: A review, Water Research (2016), doi: 10.1016/
j.watres.2016.03.003.
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Compactness and Flexible and novel
portability reactor designs
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Wavelength Tailored irradiation for
diversity improved inactivation
UV-LED
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Water
Adjustable pulsed Selected frequency for disinfection
illumination enhanced disinfection
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2 disinfection: A review
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4 Department of Chemical and Biological Engineering, The University of British Columbia, 2360
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5 East Mall, Vancouver, BC V6T 1Z3, Canada
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Corresponding author. Tel.: +1 (604)822 1902; fax: +1 (604) 822 6003.
E-mail address: fariborz.taghipour@ubc.ca (F. Taghipour).
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6 Abstract
8 water and is of growing interest for industrial application. A new UV source — ultraviolet light-
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9 emitting diode (UV-LED) — has emerged in the past decade with a number of advantages
10 compared to traditional UV mercury lamps. This promising alternative raises great interest in the
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11 research on application of UV-LEDs for water treatment. Studies on UV-LED water disinfection
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12 have increased during the past few years. This article presents a comprehensive review of recent
13 studies on UV-LEDs with various wavelengths for the inactivation of different microorganisms.
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14 Many inconsistent and incomparable data were found from published studies, which underscores
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15 the importance of establishing a standard protocol for studying UV-LED inactivation of
17 observed in the literature for some microorganisms, which requires further investigation for a
20 wavelengths and pulsed illumination; however, more studies are needed to investigate the
influencing factors and mechanisms. The special features of UV-LEDs offer the flexibility of
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24 inactivation effectiveness
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26 1. Introduction
28 countries and rural areas. Millions of people around the world lack access to a safe drinking
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29 water source and are threatened by waterborne diseases annually (Hatami, 2013; WHO, 2014).
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31 microorganisms in water, is of great significance for human health and well-being.
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32 Ultraviolet (UV) radiation can effectively inactivate various microorganisms in water
33 (Hijnen et al., 2006) and has been increasingly used for water disinfection. UV radiation has
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34 numerous advantages over conventional chemical disinfection (e.g., chlorination or ozonation),
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35 such as no chemical addition, no harmful disinfection by-products (DBPs) formation, and no
37 recommended as a substitute for chemical additives for surface water treatment (USEPA, 2006).
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38 Currently, there are more than 7,000 municipal UV disinfection installations in the world (Muller,
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39 2011), and small household UV disinfection systems are also available (Brownell et al., 2008). It
40 is estimated that the global market for UV disinfection equipment has a potential to reach $2.8
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41 billion by 2020 (Allied Analytics LLP, 2014). The main UV sources for current UV disinfection
42 systems are low- or medium-pressure mercury lamps (Chevremont et al., 2013a). Although these
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43 lamps are widely used in water treatment systems, there are still many issues with them. The
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44 major concern is that the UV lamps are fragile and contain toxic mercury, which is hazardous to
45 the environment and requires proper disposal (Chevremont et al., 2013b; Close et al., 2006).
46 Moreover, these lamps require significant amounts of energy to operate due to a low wall plug
47 efficiency of around 15–35% and have a relatively short lifetime of about 10,000 hours (Autin et
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49 In the past few years, with the rapid development and improvement of the semiconductor
50 industry, UV light-emitting diodes (UV-LEDs) have emerged as a new source for UV radiation
52 p-n junction (hole and electron). The electrons and holes recombine at the junction to emit
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53 radiation, and the wavelength of the radiation depends on the semiconducting materials.
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54 Commercial visible LEDs have been available for nearly 50 years and have diverse applications,
55 especially in the lighting industry, due to the increasingly higher efficiency and lower cost
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56 (Ibrahim et al., 2014). Recently, the newly emerging UV-LEDs have followed a similar track and
57 are expected to be economically viable in the coming years (Harris et al., 2013).
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58 UV-LEDs at various wavelengths can be manufactured using different semiconducting
59 materials. The most frequently used materials are III-nitride, including gallium nitride (GaN),
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60 aluminium gallium nitride (AlGaN), and aluminum nitride (AlN) (Khan et al., 2005). The
61 wavelength of GaN-based UV-LEDs can be as short as 365 nm, which is in the near UV region
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62 (Taniyasu et al., 2006b). However, the AIN UV-LEDs are reported to emit UV radiation at 210
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63 nm (deep UV), which is the shortest wavelength among semiconductors (Taniyasu et al., 2006a).
64 A wavelength from 210 to 365 nm (covering from deep UV to near UV regions) is available
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65 from the emission of AlGaN, which consists of AIN and GaN in appropriate proportions
(Taniyasu and Kasu, 2010). Because the wavelength is found to be an essential factor for water
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66
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67 disinfection efficiency (Vilhunen et al., 2009), the ability of UV-LEDs to offer a variety of
68 wavelengths is well aligned with the needs of efficient disinfection, making it a potential option.
70 as environmental friendliness (no mercury), compactness and robustness (more durable), faster
71 start-up time (no warm-up time), potentially less energy consumption, longer lifetime, and the
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72 ability to turn on and off with high frequency (Wurtele et al., 2011). It is predicted that by 2020,
73 UV-LEDs will operate at 75% wall plug efficiency with a lifetime longer than 100,000 hours,
74 comparable to the operating parameters of current visible LEDs (Autin et al., 2013; Ibrahim et al.,
75 2014). All these factors make UV-LEDs a promising alternative to conventional UV mercury
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76 lamps for water disinfection. However, due to the substantial differences between the traditional
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77 mercury lamps and newly emerging UV-LEDs, the numerous research results and established
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79 designs, and inactivation kinetics, may not apply directly to UV-LEDs. Moreover, few studies
80 currently exist that investigate the application of UV-LEDs to water disinfection. Therefore, a
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comprehensive research on UV-LEDs for water disinfection is essential to better understand the
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82 feasibility and future applications of this technology.
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83 This review presents and discusses published data from the literature, aiming to give an
84 overall understanding of UV-LED water disinfection. Using the results of this review, some of
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85 the main future research directions are identified. To the best of the authors’ knowledge, this is
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86 the first review paper on the application of newly emerging UV-LEDs for water disinfection.
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88 There has been a lack of uniformity in research materials and methods reported for UV-
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89 LED disinfection studies over the last decade, making comparisons difficult. Table 1 summarizes
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90 the main results from the published work on UV-LED water disinfection. The data on UV dose
91 and log inactivation were obtained from each study, and the UV dose response, as the value of
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(unit: mJ/cm2 per log inactivation), was calculated to evaluate and compare the
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95 wavelength, and the spectral sensitivity of microorganisms was found to not necessarily follow
96 the DNA absorbance spectrum (Chen et al., 2009, Mamane-Gravetz et al., 2005). Therefore, UV
97 wavelength is an essential factor for microorganism inactivation, and the effectiveness may vary
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98 from microorganism to microorganism (Linden et al., 2001, Vilhunen et al., 2009). Different UV
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99 wavelengths in the range of 315–400 nm (UVA), 280–315 nm (UVB), and <280 nm (UVC) have
100 been applied for microorganism inactivation by UV-LEDs. From the published data, sorted by
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101 wavelength (Table 1), the influence of UV-LED wavelengths on inactivation effectiveness can
102 be evaluated.
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103 Hamamoto et al. (2007) and Mori et al. (2007) applied UVA radiation with 365-nm UVA-
104 LEDs on E. coli and obtained UV dose responses of 55,263 and 13,846 mJ/cm2 per log
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105 inactivation, respectively (Table 1). These values are high considering that typically the UV dose
106 required by 254-nm mercury lamps for 4 log E. coli inactivation is about 8 mJ/cm2, which makes
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107 the UV dose response only 2 mJ/cm2 per log inactivation (Bolton and Cotton, 2008). With the
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108 help of titanium dioxide (TiO2), Xiong and Hu (2013) established a photocatalytic disinfection
109 system using 365-nm UV-LEDs, and the results still showed a high UV dose response of 229
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110 mJ/cm2 per log inactivation for E. coli inactivation. These results demonstrated that 365-nm
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112 Oguma et al. (2013) used 310-nm UVB-LEDs for E. coli inactivation and reported a UV
113 dose response of 94.8 mJ/cm2 per log inactivation, which is much lower than that required for
114 365-nm UVA-LEDs. Nonetheless, this result was far greater than the values reported for UVC-
115 LEDs for various microorganisms, which ranged from 1.0 to 30.5 mJ/cm2 per log inactivation
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116 (Table 1). Therefore, UVB-LEDs alone are also not highly effective for microorganism
117 inactivation.
118 Aoyagi et al. (2011) selected 255-nm and 280-nm UVC-LEDs to study the inactivation
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119 effects on bacteriophages φX174, Qβ, and MS2. The results showed that the UV dose responses
120 at 280 nm for these three microorganisms were 2.8, 28.7, and 30.5 mJ/cm2 per log inactivation,
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121 respectively (Table 1), which were all higher than those at 255 nm (1.7, 12.5, and 12.8 mJ/cm2
122 per log inactivation, respectively). The results indicated that UVC-LEDs at 255 nm could be
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123 more effective than at 280 nm for the inactivation of bacteriophages φX174, Qβ, and MS2.
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124 Another study on UVC-LEDs at 255 nm and 275 nm was reported by Bowker et al. (2011)
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125 for the inactivation of three microorganisms: MS2, T7, and E. coli. Similar UV dose responses
126 were obtained from this study for the 255-nm and 275-nm wavelengths (26.1, 5.1, and 3.3
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127 mJ/cm2 per log inactivation versus 28.6, 4.3, and 2.4 mJ/cm2 per log inactivation for MS2, T7,
128 and E. coli, respectively; Table 1). For MS2, the UV dose response at 255 nm was slightly lower
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129 than that at 275 nm, indicating that UVC-LED at 255 nm was more effective than at 275 nm.
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130 However, for T7 and E. coli, 255 nm resulted in slightly higher UV dose responses than at 275
131 nm, suggesting that 275 nm was more effective. The results for MS2 and T7 were consistent with
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132 their action spectra, considering that the action spectrum of MS2 has a peak around 260 nm and
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133 the peak for T7 is around 270 nm (Mamane-Gravetz et al., 2005, Ronto et al., 1992, Beck et al.,
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134 2015). The results did not agree with the E. coli action spectrum given that 255 nm is closer to
135 the peak around 260–265 nm and therefore 255 nm is expected to be more effective than 275 nm
136 (Bolton and Cotton, 2008). The higher effectiveness of 275 nm may be attributed to the higher
137 output power of the 275-nm UV-LEDs, resulting in a higher fluence rate and shorter exposure
138 time to reach the same UV dose, which is proposed to be more effective for E. coli inactivation
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139 than the combination of a lower fluence rate and longer exposure time (Bowker et al., 2011,
140 Harm, 1980, Sommer et al., 1998). Basically, UV inactivation of microorganisms is believed to
141 follow the Bunsen–Roscoe reciprocity law, which states that the photochemical effect depends
142 only on the total energy dose, i.e., the product of fluence rate and exposure time (Murata and
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143 Osakabe, 2013). This was verified by Sommer et al. (1998) who reported that for inactivation of
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144 bacteriophages MS2, φX174, and B40-8 by mercury UV lamps, log inactivation is the same as
145 long as the product of fluence rate and exposure time is the same. At the same time, these authors
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146 found a deviation from the reciprocity law for E. coli inactivation that showed a higher fluence
147 rate and shorter exposure time resulted in a higher log inactivation than a lower fluence rate and
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a longer exposure time despite the total UV fluence (UV dose) being the same. This phenomenon
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149 could be attributed to UV disinfection depending not only on photochemical reactions but also
on biological processes (Harm, 1980). Therefore, the deviation from the reciprocity law may
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151 occur on certain microorganisms, like E. coli, because the biological processes induced by UV
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152 radiation may vary with different microorganisms, and some of the organisms may be more
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154 Although some of the UV-LED dose responses reported from different studies are in
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155 agreement, there are many cases where the results are inconsistent. One such example is the
inconsistency in results between studies by Aoyagi et al. (2011) and Bowker et al. (2011). Both
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156
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157 studies used 255-nm UVC-LEDs for MS2 inactivation. However, in the former case, a 41-
158 mJ/cm2 UV dose provided a 3.2 log inactivation, whereas in the latter, a 60-mJ/cm2 UV dose
159 achieved only 2.3 log inactivation. Similar inconsistent results were also observed between the
160 studies by Chatterley and Linden (2010) and Oguma et al. (2013), where both applied 265 nm to
161 E. coli and reported UV dose responses of 5.9 and 2.7 mJ/cm2 per log inactivation, respectively.
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162 These disagreements might result from the differences among materials and experimental
163 conditions in the different studies. Different UV-LEDs in these studies have various radiation
164 patterns, such as emission spectra, viewing angle, and radiation distribution. Various apparatuses
165 were applied for UV-LED water disinfection, and different methods were used to determine the
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166 UV dose from the UV-LEDs. Currently, there is no consistent methodology for obtaining the
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167 UV-LED dose response of microorganisms, and there is no standard protocol for determining the
168 UV dose delivered by UV-LEDs to a sample solution. Therefore, the discrepancy among
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169 different studies is inevitable.
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170 The standardized protocol for microorganism inactivation by conventional UV mercury
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171 lamps has been well established, and the results under the standardized procedure are comparable
172 (Bolton and Linden, 2003, Kuo et al., 2003). However, the UV lamp protocol is not expected to
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173 be directly applicable to UV-LEDs because of the substantial differences between mercury lamps
174 and UV-LEDs. The bench-scale UV disinfection experiments for mercury lamps usually utilize a
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175 collimated beam apparatus (Fig.1A). The key part of this apparatus—a collimated beam—is used
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176 to provide a uniform irradiation field on a surface area by collimating a parallel beam to
177 vertically project on the water surface, so that the irradiance on the surface of the sample can be
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178 accurately measured by a radiometer, enabling the UV dose to be determined with necessary
corrections (Bolton and Linden, 2003). To ensure the uniformity of the beam and accuracy of the
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179
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180 measurement, the length of the collimated beam has to be at least 20 cm (Blatchley, 1997). Such
181 a long collimated beam is not practical for UV-LEDs due to their low radiant power. Currently,
182 the output power of a UVC-LED is only several milliwatts, which is much lower than that of
184 lamps (up to 30 kW). As a result, the UV-LEDs have to be close to a water sample in which
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185 inactivation is performed for deliverable UV energy. Various apparatus can be applied for UV-
186 LED inactivation of microorganisms. Typically, the UV-LEDs are located directly above the
187 water sample (Fig.1B), and the distance between UV-LEDs and the water sample is usually no
188 more than 2 cm (Chevremont et al., 2012a, Chevremont et al., 2012b, Hamamoto et al., 2007,
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189 Hwang et al., 2013, Li et al., 2010, Mori et al., 2007, Oguma et al., 2013, Vilhunen et al., 2009).
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190 Considering that a UV-LED is a point source and emits hemispheric radiation, the UV emission
191 from a UV-LED is neither parallel nor vertical to the water surface within such a short distance
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192 between the UV-LED and the water sample (Fig.1B). As a result, uniform irradiance is not
193 expected on the water sample surface, which leads to difficulties for the accurate determination
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of UV dose. Further, the radiant power of UV-LEDs can be significantly affected by operating
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195 parameters, such as the applied current and voltage, and by thermal management during the
operation. Therefore, there is a need for the development of a standardized protocol for a UV-
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197 LED-based inactivation study of microorganisms, especially for the accurate determination of
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198 UV dose and the proper operation of the system. This necessity has been recognized by
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199 researchers and industry leaders in the field of UV-LEDs. Recently, an International Ultraviolet
200 Association (IUVA) initiative has been announced, undertaken by a working group of the IUVA
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201 Manufacturers Council, to present a consistent methodology for the determination and
203 Chevremont et al. (2012a) studied the inactivation effect of coupled UVA- and UVC-LEDs
204 on mesophilic bacteria. The UV dose responses for UVA alone at 365 nm and 405 nm were 12.5
205 and 88 mJ/cm2 per log inactivation, which are much higher than those for the UVC alone at 254
206 nm and 280 nm (both 1.0 mJ/cm2 per log inactivation). However, when combining UVA- and
207 UVC-LEDs, the UV dose responses at 254/365 nm, 280/365 nm, 254/405 nm, and 280/405 nm
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208 all sharply decreased (2.1, 1.6, 11.9, and 7.7 mJ/cm2 per log inactivation, respectively),
209 indicating that the combination of UVA- and UVC-LEDs is more efficient than UVA-LEDs
210 alone. Moreover, in terms of log inactivation, it was found that the combination of 280 nm and
211 365 nm provided higher log inactivation than the sum of each alone (3.5 > 1.4 + 0.3 = 1.7). The
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212 other three combinations showed similar phenomena: 254/365 nm (2.4 > 0.8 + 0.3 = 1.1),
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213 254/405 nm (2.2 > 0.8 + 0.3 = 1.1), and 280/365 nm (3.5 > 1.4 + 0.3 = 1.7). This synergistic
214 effect from the wavelength combinations was also reported by Nakahashi et al. (2014), who
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215 combined 254 nm with 365 nm for Vibrio parahaemolyticus inactivation. However, Oguma et al.
216 (2013) combined 265-nm, 280-nm, and 310-nm UV-LEDs for E. coli inactivation and did not
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observe a synergistic effect. On the contrary, these researchers found that combined wavelengths
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218 were less efficient than each wavelength applied separately, which could have resulted from
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220 thermal management of the experimental setup (Oguma et al., 2013). These studies suggest that
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221 combination of selected wavelengths might be a promising way to improve the disinfection
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222 efficiency of UV-LEDs, but more studies are needed because the experimental setup and
224 Although a medium-pressure mercury lamp can provide polychromatic radiation, its
spectrum, which includes UVA, UVB, UVC, and visible light, is fixed and cannot be adjusted.
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225
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226 Different effects and mechanisms for medium-pressure mercury lamp inactivation of
227 microorganisms have been attributed to its polychromatic radiation. However, within the very
228 broad range of wavelengths in its spectrum, it is difficult to identify and distinguish which
229 wavelength or which combination of specific wavelengths the additional effects and mechanisms
230 result from. UV-LEDs provide great flexibility for wavelength combinations and fluence rate
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231 due to their unique feature of wavelength diversity. This flexibility offers a new approach to
232 tailor wavelength combinations and the radiant power of each peak wavelength for optimal
233 inactivation and to identify the additional mechanism of a particular combination and fluence
234 rate.
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235 The ability to turn on and off with a high frequency is another unique feature of UV-LEDs,
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236 enabling adjustable UV pulsed illumination. Such a feature makes UV-LEDs desirable for
237 potentially enhancing the inactivation effectiveness by pulsed irradiation. Li et al. (2010)
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238 reported enhanced germicidal effects of pulsed UV-LED irradiation by applying UVA-LED at
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239 365 nm for inactivation of Candida albicans and E. coli biofilms. They found that pulsed
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240 irradiation had significantly greater germicidal ability than continuous irradiation with a
241 maximum at 100 Hz and 75% duty rate (the percentage of the exposure time in total operating
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242 time) under the same UV dose. Wengraitis et al. (2013) applied pulsed UVC radiation by UV-
243 LEDs at 272 nm for E. coli disinfection on agar plates and found it to be more effective than
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244 continuous illumination; the log inactivation for pulsed UVC radiation at 272 nm with 1 Hz and
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245 10% duty rate was 3.8 times higher than that of continuous illumination based on the same UV
247 The conventional UV source for generating pulsed UV is a xenon lamp. The enhanced
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248 germicidal effect of xenon lamp-pulsed UV has been demonstrated by studies for food
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249 decontamination and water disinfection (Bohrerova et al., 2008, Elmnasser et al., 2007, Gomez-
250 Lopez et al., 2007, Oms-Oliu et al., 2010). However, the pulses generated by a xenon lamp are
251 different from those of UV-LEDs in terms of spectrum, intensity, frequency, and duty rate. The
252 wavelength distribution of xenon lamp pulses ranges from 100 nm to 1000 nm, including UV,
253 visible light, and infrared with a peak power up to 35 MW. Usually the duration of each pulse is
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254 from nanoseconds to milliseconds, and typically 1 to 20 pulses are emitted per second (Oms-Oliu
255 et al., 2010). As discussed previously, UV-LEDs have selectable wavelengths with relatively low
256 radiant power and are capable of highly adjustable pulsed illumination with broad ranges for
257 frequency and duty rate. The numerous studies on xenon lamp-pulsed UV reveal that these pulse
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258 patterns play important roles for enhanced germicidal effect (Elmnasser et al., 2007). Therefore,
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259 due to the differences in pulse patterns, the direct applicability of the findings on xenon lamp-
260 pulsed UV to UV-LED pulsed illumination is not expected, and more studies on UV-LED pulsed
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261 illumination are needed to confirm the enhanced germicidal effect.
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262 3. Microorganism response to UV-LEDs AN
263 Although UV radiation is effective against most pathogenic microorganisms in water,
264 different microorganisms have different responses to UV radiation due to various UV resistances
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265 and process conditions. The sensitivity of microorganisms to UV radiation can be evaluated by
the inactivation rate constant k (cm2/mJ) from the linear portion of the relationship between log
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269 The k values for various microorganisms were calculated based on the data from each study
270 (summarized in Table 1), and are listed in Table 2. The data from conventional UV mercury
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271 lamps at 254 nm are also shown in Table 2 for comparison. A high k value means the
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273 The k values for bacteriophage φX174 by 255-nm and 280-nm UV-LEDs were reported as
274 0.578 and 0.360 cm2/mJ, respectively (Aoyagi et al., 2011), which were higher than all other
275 microorganisms in Table 2, suggesting that φX174 is very vulnerable to UVC radiation. The k
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276 value for φX174 by 254 nm was also much higher than that for most of the other microorganisms
277 in the studies concerning UV lamps. However, the k value of UV lamps at 254 nm was closer to
278 that of UV-LEDs at 280 nm instead of 255 nm. This disagreement may result from the
279 differences between these two UV sources, including the fact that the UV fluence rate of
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280 conventional UV lamps is much higher than that for UV-LEDs, which may affect the
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281 microorganism responses (Harm, 1980). On the other hand, φX174 inactivation by UV lamps
282 showed no sensitivity to different fluence rates based on the study by Sommer et al. (1998).
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283 Nonetheless, further research is needed to investigate the UV-LED wavelength effect given the
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285 E. coli inactivation was investigated with UVC-LEDs at different wavelengths (255, 265,
286 272, 275, and 280 nm) in several studies (Bowker et al., 2011, Chatterley and Linden, 2010,
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287 Oguma et al., 2013, Wengraitis et al., 2013). The k values ranged from 0.170 to 0.422 cm2/mJ,
288 which were slightly lower than the values for φX174, indicating that E. coli is quite sensitive to
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289 UVC radiation. The wide range of k values suggests that UV sensitivity of E. coli largely
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290 depends on the wavelength. Moreover, although these studies used E. coli as the indicator
291 microorganism, the strains of E. coli were different, which could be a factor that results in the
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292 different inactivation rate constants because UV sensitivity may vary with different strains of a
species, especially for E. coli (Malley, 2004, Sommer et al., 1998, Sommer et al., 2000). The
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average k value from UV lamp studies for E. coli inactivation was 0.506 cm2/mJ, which was
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295 higher than the values found using UV-LEDs, with 275 nm resulting in the closest value, rather
296 than the 255-nm UV-LED. A possible explanation may be the difference of fluence rate from
297 UV lamps and UV-LEDs since a few studies have found that the fluence rate can affect E. coli
298 inactivation (Bowker et al., 2011, Harm, 1980, Sommer et al., 1998). As previously discussed,
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299 although UV-LEDs are usually placed very close to the water sample for UV exposure (Fig. 1),
300 the fluence rate is still much lower than that of UV lamps due to the low output power of current
301 UV-LEDs, which could be an influencing factor. Bowker et al. (2011) compared a 254-nm UV
302 lamp with 275-nm and 255-nm UV-LEDs for E. coli inactivation. The fluence rates were 0.34,
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303 0.094–0.11, and 0.049–0.060 mW/cm2, respectively. The results showed that log inactivation for
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304 the same UV dose increased concurrently with the increase in fluence rate: from the 255-nm UV-
305 LED to the 275-nm UV-LED to the 254-nm UV lamp. These results support the hypothesis that
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306 the combination of a higher fluence rate and shorter exposure time may result in higher E. coli
307 inactivation as previously discussed, which could explain the influence of different UV sources.
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Bacteriophage T7 was found to have k values of 0.195 and 0.235 cm2/mJ by 255-nm and
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309 275-nm UV-LEDs, respectively (Bowker et al., 2011), which were slightly lower than those of E.
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310 coli, indicating that T7 was also sensitive to UVC radiation. The k value for 275 nm was slightly
311 higher than that of 255 nm, suggesting that T7 was more sensitive to 275 nm than to 255 nm, in
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312 agreement with the action spectrum of T7 bacteriophage with a peak around 270 nm (Ronto et al.,
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313 1992, Beck et al., 2015). The k value of a UV lamp for T7 was 0.232 cm2/mJ, which was close to
314 that found with the 275-nm UV-LED but far from the 255-nm UV-LED, implying that T7 may
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316 Bacillus subtilis spores were inactivated in two studies (Morris, 2012, Wurtele et al., 2011)
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317 by UV-LEDs with three different wavelengths (250, 269, and 282 nm). The k values for 269 nm
318 and 282 nm were 0.148 and 0.120 cm2/mJ, respectively, but the k value decreased dramatically
319 to 0.051 cm2/mJ for 250 nm. These results seemed to be related to the action spectrum of
320 Bacillus subtilis spores, which have a peak around 265 nm and a trough around 240 nm
321 (Mamane-Gravetz et al., 2005). The k value for Bacillus subtilis spores by a UV lamp was 0.059
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322 cm2/mJ, which was similar to that of a 250-nm UV-LED, showing a consistency in the UV
323 sensitivity of Bacillus subtilis spores between the two different UV sources.
0.080 and 0.035 cm2/mJ, respectively (Aoyagi et al., 2011), which were lower than most of the
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326 microorganisms listed in Table 2, indicating that bacteriophage Qβ was highly resistant to UVC
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327 radiation. The k value at 255 nm was significantly higher than that at 280 nm, which agreed well
328 with the action spectrum of Qβ having a peak between 260 and 265 nm (Beck et al., 2015). The k
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329 value for the 255-nm UV-LED agreed well with the values from low-pressure UV lamp
inactivation studies for Qβ (0.084 cm2/mJ), implying that Qβ had the same UV sensitivity at
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331 different UV sources.
332 Bacteriophage MS2 inactivation was reported in two studies (Aoyagi et al., 2011, Bowker et
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333 al., 2011) using UV-LEDs at three different wavelengths (255, 275, and 280 nm). The k values
334 for 280 nm from the former study and 255, 275 nm from the latter study were close (0.033, 0.038,
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335 and 0.035 cm2/mJ, respectively) and among the lowest of all the microorganisms inactivated by
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336 UVC radiation, indicating that MS2 was highly resistant to UVC radiation. The k value for 255
337 nm from the former study was 0.078 cm2/mJ, which was higher than the other values. This result
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338 matched the action spectrum of MS2, which has a peak around 260 nm (Mamane-Gravetz et al.,
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339 2005, Beck et al., 2015). Although these two studies showed different k values for the 255-nm
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340 UV-LED on MS2 inactivation, the average was 0.058 cm2/mJ, which was close to that for MS2
341 inactivation by conventional UV lamps (0.055 cm2/mJ). This finding suggested that MS2 might
342 also be insensitive to different fluence rates from UV-LEDs and conventional UV lamps.
343 These studies have demonstrated the diversity of UV responses for different
344 microorganisms to various wavelengths. Because UV response largely depends on the indicator
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345 microorganisms and applied wavelength by UV-LEDs, a particular wavelength could be much
346 more effective for a specific microorganism. Unlike UV lamps, UV-LEDs can be designed to
347 emit a particular wavelength that targets a specific pathogen of concern. In addition, the selected
348 wavelengths could be combined by applying various UV-LEDs to produce a synergistic effect
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349 (Taghipour, 2013). Therefore, a comprehensive investigation of microorganism responses to
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350 UV-LEDs with different wavelengths and wavelength combinations is essential to take full
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352 Additionally, from the comparison with conventional UV mercury lamps at 254 nm, some
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353 microorganisms showed different UV sensitivities to different UV sources at the same
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354 wavelength, indicating that the characteristics and performance of UV sources, such as the
355 fluence rate, may play important roles in microorganism inactivation. Microorganisms were
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356 previously shown to exhibit higher UV sensitivities to medium-pressure mercury lamps than to
357 low-pressure mercury lamps (Hijnen et al., 2006). However, few studies compare UV-LEDs and
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358 UV lamps. Thus, more studies are required to better understand how different UV sources affect
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360
361 Some studies reported time-response data for microorganism inactivation by UV-LEDs
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362 instead of dose-response data (Table 3). The UV exposure times ranged from 30 seconds to 2
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363 hours, and log inactivation ranged from 2 to 7; both results showed a wide range and seemed
364 incomparable. Because no quantitative data on UV dose were provided in these studies, it was
365 difficult to analyze and compare the effectiveness of UV-LED inactivation. The difficulty was
366 most likely caused by the lack of an established standard method for the measurement of UV
367 dose associated with the newly emerging UV-LEDs, which are substantially different from UV
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368 mercury lamps as discussed previously. This issue demonstrates the significance of UV-LED
369 characterization and the need for standard protocols for UV-LED microorganism inactivation
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371 5. Mechanism of inactivation
372 Many studies have discussed the mechanism of microorganism inactivation by UV-LEDs,
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373 and various mechanisms have been proposed. Much like the conventional mercury-based UV
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374 lamps, UVC radiation has proven to be efficient for microorganism inactivation, and most
375 studies on UV-LED disinfection used UVC-LEDs. UVC radiation is believed to have direct
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376 germicidal effects by acting directly on the DNA of microorganisms, leading to the formation of
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377 pyrimidine dimers and preventing them from reproducing without intermediate steps (Chatterley
378 and Linden, 2010, Chevremont et al., 2012a, Chevremont et al., 2012b, Hamamoto et al., 2007).
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379 Because DNA mainly absorbs UV radiation from 200 to 300 nm with an absorbance peak around
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380 260 nm (Wurtele et al., 2011), UVC-LEDs, especially those with the wavelengths around 260
381 nm, are the most efficient for microorganism inactivation (Table 1). However, direct damage to
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382 DNA might be reparable by DNA-repair mechanisms, such as photo-reactivation and dark repair
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383 (Oguma et al., 2001, Oguma et al., 2013, Sanz et al., 2007). Since DNA repair is undesirable for
384 microorganism inactivation, it is necessary to weaken or prevent the repair. DNA repair might be
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385 prevented by damaging the repair enzymes, which are proposed to be more vulnerable to high
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386 UV intensities (Sommer et al., 1998). Moreover, the absorption spectrum of protein has a peak
387 around 280 nm, which might help damage repair enzymes and prevent DNA repair (Kalisvaart,
388 2004).
389 Although UVA radiation is poorly absorbed by DNA and is less efficient in inducing
390 damage on DNA (Sinha and Hader, 2002), it still has the ability to inactivate microorganisms
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391 (Kalisvaart, 2004). The current commercially available UVA-LEDs have much higher output
392 power and energy efficiency than UVC-LEDs (Aoyagi et al., 2011, Harris et al., 2013,
393 Muramoto et al., 2014), resulting in many studies on the application of UVA-LEDs for
394 microorganism inactivation. The inactivation mechanism of UVA radiation has not been studied
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395 as widely as UVC radiation because the frequently used UV mercury lamps can only emit UVC
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396 radiation at 254 nm. The main mechanism of UVA inactivation involves an indirect effect by
397 reactive intermediates and oxidative damage to DNA and other cellular components (Chatterley
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398 and Linden, 2010, Chevremont et al., 2012a, Chevremont et al., 2012b, Hamamoto et al., 2007,
399 Hwang et al., 2013). The reactive intermediates are proposed to be reactive oxygen species
400
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(ROS), which are created by UVA radiation via photooxidation of oxygen. Studies showed that
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401 addition of mannitol and catalase significantly protected microorganisms from 365-nm UVA-
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402 LEDs radiation by scavenging hydroxyl radicals (OH•) and hydrogen peroxide (H2O2),
403 respectively. Therefore, hydroxyl radicals and hydrogen peroxide are believed to be the major
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404 reactive oxygen species involved in UVA disinfection (Hamamoto et al., 2007, Li et al., 2010).
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405 These reactive intermediates induce oxidative damage to DNA, proteins, and cell membranes
406 and cause growth delay (Eisenstark, 1987, Oppezzo and Pizarro, 2001, Pizarro, 1995, Pizarro
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407 and Orce, 1988, Ramabhadran and Jagger, 1976, Sinha and Hader, 2002). This process takes
408 more time than the direct damage produced by UVC radiation (Chatterley and Linden, 2010).
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409 Although the indirect damage by UVA radiation is less efficient than the direct damage by UVC
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410 radiation for microorganism inactivation, the damage by UVA is believed to be irreparable,
411 whereas the damage by UVC is reparable through DNA-repair mechanisms (Oguma et al., 2013,
412 Xiong and Hu, 2013). UV damage by low-pressure mercury lamps, which emit UVC radiation at
413 254 nm, can be repaired relatively easily, but UV damage induced by medium-pressure mercury
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414 lamps, which produce UVC and UVA radiation together, is difficult to repair (Oguma et al.,
415 2002, Zimmer and Slawson, 2002). Therefore, the prevention of microorganism self-repair
416 would be an advantage of UVA radiation for microorganism inactivation. Furthermore, UVA
417 radiation has higher penetrability and can penetrate farther into the solution for a better
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418 disinfection of turbid water and wastewater (Chevremont et al., 2012a, Mori et al., 2007).
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419 UVA radiation alone is less efficient for disinfection, but UVA radiation coupled with TiO2
420 could efficiently produce reactive oxygen species for microorganism inactivation (Marugan et al.,
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421 2010). Because UVA-LEDs have high output power, they are desirable for photocatalytic
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422 disinfection with TiO2. An interesting phenomenon called “residual disinfecting effect” was
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423 reported, in which further inactivation of E. coli was observed after a photocatalytic process
424 using a combination of UVA-LEDs and TiO2 (Xiong and Hu, 2013). The mechanism for residual
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425 disinfecting effect was proposed to be the cumulative damage of cellular components by reactive
426 oxygen species or stable oxidants, such as H2O2, which could prevent the reproduction of
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427 damaged microorganisms (Pablos et al., 2013, Rincon and Pulgarin, 2004, 2007, Shang et al.,
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428 2009).
429 Many studies have been conducted on microorganism inactivation mechanisms using
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430 different wavelengths, including UVC and UVA, with a focus on the effect on DNA damage.
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431 However, there is little information in the literature on DNA damage and inactivation
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432 mechanisms using a combination of different UV wavelengths (Nakahashi et al., 2014). Because
433 a few studies have reported the synergistic effect of combining particular wavelengths
434 (Chevremont et al., 2012a, Nakahashi et al., 2014), identifying the mechanisms is essential.
435 Chevremont et al. (2012a) argued that coupled wavelengths combined two UV properties: UVC
436 induces direct damage on DNA, but such DNA damage can be repaired by enzyme photolyase,
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437 whereas the oxidative damage to bacterial membranes by UVA cannot be repaired. The research
439 UVA alone, and a thymine dimer, cyclobutane pyrimidine dimers (CPDs), which was induced by
440 UVC alone, suggested that the combination of UVA and UVC suppressed one or more recovery
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441 systems for DNA damage, such as CPDs, and oxidative stress from UVAs may play a key role in
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442 this synergistic effect (Nakahashi et al., 2014). It is proposed that the coupled wavelengths of
443 UVA and UVC may also reduce reactivation after exposure due to the combined effects of two
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444 types of UV wavelengths (Chevremont et al., 2012a).
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445 The mechanism of pulsed UV illumination by xenon lamps with high energy and a broad
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446 spectrum has been widely studied for inactivation and food decontamination. Yet, its effect is not
447 well understood, and there is little research on pulsed illumination by UV-LEDs. Pulsed UV
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448 illumination has more instantaneous energy than continuous UV illumination (Li et al., 2010),
449 and additional inactivation mechanisms have been proposed, including photochemical,
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450 photothermal, and photophysical effects (Elmnasser et al., 2007). Other than DNA damage by
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451 UV, it is believed that pulsed UV treatment can prevent DNA repair due to inactivation of the
452 DNA-repair system and other enzymatic functions (Elmnasser et al., 2007). The UV pulse with
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453 more instantaneous energy may lead to localized overheating and membrane destruction
(Krishnamurthy et al., 2007). Furthermore, the repeated and constant disturbance from high
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454
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455 intensity pulses could induce cell structure damage such as cell wall rupture, membrane damage,
456 and cellular content leakage (Krishnamurthy et al., 2010). As a result of these additional effects,
457 pulsed UV illumination is reported to be 4 to 6 times faster than continuous UV illumination for
458 equivalent inactivation levels (Fine and Gervais, 2004). These proposed mechanisms are mainly
459 based on studies of xenon lamps pulsed UV illumination with high energy and a broad spectrum.
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460 Due to the different pulses generated by xenon lamps and UV-LEDs, the applicability of these
461 mechanisms for UV-LED pulsed illumination still needs further examination.
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463 The research on water disinfection by newly emerging UV-LEDs is limited. Because UV-
464 LEDs are believed to be a promising alternative to traditional UV mercury lamps (Muramoto et
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465 al., 2014), more research is required to better understand the application of UV-LEDs for water
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466 disinfection. Further, some unique features of UV-LEDs such as wavelength diversity and pulsed
467 illumination and their effects on microorganism inactivation must be explored and understood.
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468 Given that UV-LEDs are compact and the radiation patterns, such as emission wavelength,
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469 viewing angle, and radiation distribution, are adjustable, they can enable creative reactor designs
470 through the optimization of flow and radiation distribution, as well as reactor geometry and
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471 kinetics (Taghipour, 2013). The following are a few suggested areas for further investigation:
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472 1) UV-LED characterization and a standard protocol for microorganism inactivation are
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474 Specifically, a standard method for UV-dose determination of UV-LEDs is essential for
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475 accurate and reliable UV dose-response data, which can be compared among different
476 studies.
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477 2) Multiple wavelengths and pulsed illumination by UV-LEDs can have significant
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478 impacts on inactivation effectiveness, but more studies are required for the fundamental
481 pulsed illumination require further investigation, which could lead to the design of more
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482 efficient disinfection systems using tailored combinations of selected wavelengths and
484 4) Research on reactor designs for UV-LED water disinfection system is highly
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485 encouraged for the practical application of this technology. The unique characteristics of
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487 robustness, wavelength diversity, and pulsed illumination, provide flexible and diverse
488 options for novel reactor designs, which could also open the door to new applications of
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489 UV-LED reactors.
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490 7. Conclusions
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491 Newly emerging UV-LEDs provide a promising alternative for water disinfection due to
492 many advantages over traditional mercury lamps. The comparison of microorganism response to
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493 UV-LEDs and conventional UV lamps reveals that some microorganisms may be sensitive to
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494 different UV sources, likely due to the difference in the UV source radiation patterns and the
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495 fluence rates. Inactivation studies of several microorganisms using UV-LED of the same
496 wavelengths and comparable fluence rates, however, still show considerable discrepancies
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497 among published results. The inconsistent and incomparable reported results on water
498 disinfection by UV-LEDs along with the substantial differences between UV-LEDs and UV
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499 lamps highlight the importance and necessity of having a standard protocol for UV-LED
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500 microbial inactivation studies, especially a standard method for UV-dose determination using
501 UV-LEDs.
502 The unique characteristics of UV-LEDs, particularly multiple wavelengths and pulsed
503 illumination, could improve inactivation effectiveness under optimal conditions. However, the
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504 influencing factors and mechanisms involved need to be further investigated for a more efficient
505 application of UV-LEDs. The special features of UV-LEDs as small-point UV sources with
506 adjustable radiation patterns provide great flexibility for novel reactor designs and new
507 applications. The design of new UV-LED reactors, however, has to be performed taking into
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508 account three phenomena: the reactor hydrodynamics, radiation distribution, and kinetics. Each
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509 of these phenomena may be implemented with a higher degree of freedom using UV-LEDs as
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511 Acknowledgements
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512 The authors are grateful to the Natural Science and Engineering Research Council
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513 (NSERC) of Canada for financial support. K. Song is also grateful for a scholarship from the
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bacteria 2012a
255 φX174 Water 6.4 3.7 1.7 Aoyagi et al., 2011
255 Qβ Water 30 2.4 12.5 Aoyagi et al., 2011
255 MS2 Water 41 3.2 12.8 Aoyagi et al., 2011
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255 MS2 Water 60 2.3 26.1 Bowker et al., 2011
255 T7 Water 20 3.9 5.1 Bowker et al., 2011
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255 E. coli Water 9 2.7 3.3 Bowker et al., 2011
Chatterley and
265 E. coli Water 20 3.4 5.9
Linden, 2010
265 E. coli Water 10.8 4 2.7 Oguma et al., 2013
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Pseudomonas Biofilm in
265 7.8 4 2.0 Bak et al., 2010
aeruginosa tube
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269 B. subtilis Water 40 5.9 6.8 Wurtele et al., 2011
275 MS2 Water 60 2.1 28.6 Bowker et al., 2011
275 T7 Water 20 4.7 4.3 Bowker et al., 2011
275 E. coli Water 9 3.8 2.4 Bowker et al., 2011
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Hamamoto et al.,
365 E. coli Water 315000 5.7 55,263
2007
365 E. coli Water 54000 3.9 13,846 Mori et al., 2007
365 E. coli Water/TiO2 688 3 229 Xiong and Hu, 2013
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bacteria 2012a
mesophilic Chevremont et al.,
405 Water 25.58 0.3 88.0
bacteria 2012a
mesophilic Chevremont et al.,
254/365 Water 4.95 2.4 2.1
bacteria 2012a
mesophilic Chevremont et al.,
280/365 Water 5.59 3.5 1.6
bacteria 2012a
mesophilic Chevremont et al.,
254/405 Water 26.31 2.2 11.9
bacteria 2012a
mesophilic Chevremont et al.,
280/405 Water 26.95 3.5 7.7
bacteria 2012a
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E. coli 11229 255 UV-LEDs 0.300 Bowker et al., 2011
Chatterley and Linden,
E. coli K12 29425 265 UV-LEDs 0.170
2010
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E. coli K12 IFO 3301 265 UV-LEDs 0.370 Oguma et al., 2013
E. coli 11229 275 UV-LEDs 0.422 Bowker et al., 2011
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E. coli K12 IFO 3301 280 UV-LEDs 0.290 Oguma et al., 2013
E. coli 254 UV lamps 0.506 Hijnen et al., 2006
T7 255 UV-LEDs 0.195 Bowker et al., 2011
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T7 275 UV-LEDs 0.235 Bowker et al., 2011
T7 254 UV lamps 0.232 Hijnen et al., 2006
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Bacillus subtilis 250 UV-LEDs 0.051 Morris, 2012
Bacillus subtilis 269 UV-LEDs 0.148 Wurtele et al., 2011
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269 E. coli Water 5 min 3-4 Vilhunen et al., 2009
276 E. coli Water 5 min 3-4 Vilhunen et al., 2009
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280 E. coli Water 30 sec 7 Chevremont et al., 2012b
365 E. coli Water 30 sec 2.7 Chevremont et al., 2012b
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365(Pulse) E. coli Biofilm 1 hour 3 Li et al., 2010
365(Pulse) Candida albicans Biofilm 1 hour 3 Li et al., 2010
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Vibrio
365 Water 6 min 1 Nakahashi et al., 2014
parahaemolyticus
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375 E. coli Biofilm 2 hours 2 Hwang et al., 2013
Streptococcus
375 Water 15 min 4 Kim et al., 2007
mutans
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(A) (B)
UV lamp
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Collimated UV-LED
beam
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Water sample
container and
stirrer
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Water sample
container and
stirrer
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Fig. 1 – Schematic diagram for typical UV lamp collimated beam apparatus (A) and UV-
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LED bench scale apparatus (B)
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Highlights
The recent studies on newly emerging UV-LEDs for water disinfection are reviewed.
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Mechanisms of microorganism inactivation by UV-LEDs are discussed.
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The special features of UV-LEDs encourage flexible and novel reactor designs.
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