UV LED Review

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Received: 21 April 2020 Revised: 29 August 2020 Accepted: 16 September 2020

DOI: 10.1111/1541-4337.12645

COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Recent advances on the application of UV-LED technology


for microbial inactivation: Progress and mechanism
Yasmine Kebbi1 Aliyu Idris Muhammad1,2 Anderson S. Sant’Ana3
Leonardo do Prado-Silva4 Donghong Liu1,4 Tian Ding1,4
1College of Biosystems Engineering and
Food Science, National-Local Joint Abstract
Engineering Laboratory of Intelligent Conventional technologies for the inactivation of microorganisms in food prod-
Food Technology and Equipment,
ucts have their limitations, especially changes in quality attributes that have led
Zhejiang Key Laboratory for Agro-Food
Processing, Zhejiang University, to quality deterioration, low consumer acceptance, impact on the environment,
Hangzhou, China and potential health hazards (carcinogens). Ultraviolet (UV) light is an emerg-
2 Department of Agricultural and
ing promising nonthermal technology employed for microbial inactivation in
Environmental Engineering, Faculty of
Engineering, Bayero University, Kano, water, liquid, and solid food products to curtail the limitations above. This review
Nigeria provides an insight into UV light-emitting diodes (UV-LEDs)’ potential as an
3Department of Food Science, Faculty of alternative to the traditional UV lamps for microbial inactivation in liquid and
Food Engineering, University of
solid media. Also, the mechanisms of inactivation of lone and combined UVA-,
Campinas, Campinas, SP, Brazil
4Ningbo Research Institute,Zhejiang
UVB-, and UVC-LEDs were discussed. The strategies utilized to improve the effi-
University, Ningbo, China cacy between the UV-LED treatments at various wavelengths were summarized.
Combining different UV-LEDs treatments at different wavelengths have a syn-
Correspondence
Tian Ding, College of Biosystems Engi- ergistic effect and suppression of microbial cell reactivation. The UV-LED-based
neering and Food Science, National-Local advanced oxidation processes (AOPs) also have high germicidal action against
Joint Engineering Laboratory of Intelligent
numerous microorganisms and are efficient for the degradation of micropol-
Food Technology and Equipment, Zhe-
jiang Key Laboratory for Agro-Food Pro- lutants. Among the UV-LEDs discussed, UVC-LED has the most antimicrobial
cessing, Zhejiang University, Hangzhou, effect with the most efficient micropollutants decomposition with regards to UV-
China.
LED-based AOPs. This review has provided vital information for future applica-
Email: tding@zju.edu.cn
tion, development, and customization of UV-LED systems that can meet the food
Funding information and water safety requirements and energy efficiency.
Conselho Nacional de Desenvolvimento
Científico e Tecnológico, Grant/Award
KEYWORDS
Numbers: #302763/2014-7, #305804/2017-
advanced oxidation processes, food safety, microbial decontamination mechanism, nonther-
0; Coordenação de Aperfeiçoamento de
mal technology, synergistic effect, UV-LEDs
Pessoal de Nível Superior, Grant/Award
Number: Code 001

1 INTRODUCTION plasma, and pulsed electric field, as alternative treatments


to the traditional heat-based treatment (Fan et al., 2019;
Nowadays, consumers’ high demand for microbiologically Hertwig, Meneses, & Mathys, 2018; Liu, Zhang, Zhao,
safe food with high nutritional and organoleptic quality Wang, & Liao, 2016; Muhammad et al., 2018; Muham-
has pushed food researchers and manufacturers to devel- mad, Xiang, Liao, Liu, & Ding, 2018; Petruzzi et al., 2017).
oped novel nonthermal technologies, such as high hydro- In past years, the interest in light treatment, especially
static pressure, ultrasound (US), ionizing radiations, cold UV light treatment, has considerably increased. UV light

Compr Rev Food Sci Food Saf. 2020;19:3501–3527. wileyonlinelibrary.com/journal/crf3 © 2020 Institute of Food Technologists
R 3501
3502 APPLICATION OF UV LEDS FOR INACTIVATION. . .

technology is widely applied in the food industry due to minum nitride/aluminum gallium nitride (AlN/AlGaN),
its decontamination efficacy with limited changes in food gallium arsenide (GaAs), gallium arsenide phosphide
quality attributes. The UV light is categorized into three (GaAsP), gallium phosphide (GaP), or indium gallium
based on its wavelength as UVA (320 to 400 nm), UVB nitride (InGaN). Due to the variation of these semicon-
(280 to 320 nm), and UVC (200 to 280 nm). The wavelength ductors material properties, LEDs can emit light at dif-
range of 200 to 280 nm for UVC is considered as the germi- ferent wavelengths that target a specific pathogen of con-
cidal range due to its direct damage to the DNA of micro- cern. In addition, they have a specific characteristic to
bial cells. The UVC light treatment is applied for the decon- simultaneously emit light at various wavelengths at the
tamination of various food products including chicken, same time (Jo & Tayade, 2014). This flexibility opens the
raw salmon, hazelnut, tiger nut milk, and tomato (Basaran, possibility to combine different LEDs wavelength that
2009; Holck, Liland, Carlehög, & Heir, 2018; Lim & Har- could lead to a probable synergistic effect for bacterial
rison, 2016; Yang, Sadekuzzaman, & Ha, 2017). It has also inactivation (Beck et al., 2017; Green et al., 2018; Naka-
been used for water disinfection and surface decontamina- hashi et al., 2014; Taghipour, 2018). Besides, combining
tion of various fruits and vegetables (Bintsis, Litopoulou- UV light treatment of different wavelengths has enhanced
Tzanetaki, & Robinson, 2000). Even though UVA and UVB microbial inactivation by repressing the repair of damaged
are less germicidal than UVC, they have been utilized for DNA (Oguma, Katayama, & Ohgaki, 2002; Poepping, Beck,
decontaminating and improving fruits and vegetable qual- Wright, & Linden, 2014). Previous studies have demon-
ity such as peach, blueberries, and spinach (Nguyen & strated the advantages and effects of UV-LED treatments,
Mittal, 2007; Santin et al., 2018). Moreover, it has been whether using a single wavelength or combined wave-
proved that UVA has a higher penetrability than UVC lengths of UVA-, UVB-, and UVC-LEDs. However, most
light. Thus, making it more suitable for the treatment of of the studies are limited to its application on water treat-
opaque liquids and biomaterials with a high absorptivity ment with the exact inactivation mechanism, and syner-
coefficient (Koutchma, Forney, & Moraru, 2009; Lian et al., gistic effects of the combined UV-LEDs wavelength still
2010). unclear.
In recent years, with the development of light technol- In addition to the combination of different UV-LED
ogy, more sophisticated, environmentally friendly, energy- wavelengths in improving the disinfection effectiveness,
efficient, and low-cost, light-emitting diodes (LEDs) were a combined UV-LED with photocatalysts (e.g., TiO2 , O3 ,
introduced as new UV light sources. LEDs are consid- H2 O2 , and Cl2 ) has received considerable attention. Such
ered potential competitors of the traditional UV light treatments are known as advanced oxidation processes
sources, including low and medium mercury pressure (AOPs). Recently, the UV-LED-based AOPs have shown
(Mori et al., 2007; Tayade, Natarajan, & Bajaj, 2009). The the potential for water and wastewater disinfection and
fundamental structure of the LEDs is based on the junc- pollutant degradation (Matafonova & Batoev, 2018; Wang
tion of two-terminal semiconductors, called p-n junction et al., 2017). This combined treatment has caused a syner-
that converts direct current into radiation (Figure 1). Vari- gistic effect on one hand by the direct exposure to UV light,
ous semiconductor materials are utilized in designing this and on the other hand, by the generation of free radicals
device. The prominent semiconductor materials reported such as hydroxyl radical (OH⋅ ) from the UV light (Li, Huo,
by Hinds, Donnell, Akhter, and Brijesh (2019) were alu- Wu, Lu, & Hu, 2018; Nyangaresi et al., 2019b; Wang, Hu,
Wang, & Hu, 2012). The generation of OH. due to UV light
exposure is considered as the vital element of AOPs. These
oxidation processes have resulted in cell membrane disrup-
tion, damaged DNA, and eventual cell death (Dalrymple,
Stefanakos, Trotz, & Goswami, 2010). However, the appli-
cation of UV-LED/AOPs for decontamination of microor-
ganisms is scarce compared to its application for microp-
ollutant removal.
This review aims to give an overview of UV-LEDs
progress in the past years and their advantage over conven-
tional mercury lamps in terms of inactivation efficacy and
energy demand. The review further discussed the mecha-
nisms of individual UVA-, UVB-, and UVC-LEDs, the use
of coupled LEDs at various wavelengths, and their combi-
nations with photocatalysts for microbial inactivation and
FIGURE 1 Schematic diagram of UV-LEDs arrangement micropollutants decomposition.
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3503

FIGURE 2 Mechanism of inactivation of combined UV-LEDs wavelength on microorganisms

2 MECHANISMS OF MICROBIAL toproducts, which are the two major DNA photoproducts
INACTIVATION BY UV LIGHT (Lindahl & Wood, 1999; Mitchell &Karentz, 1993; Yeo &
Liong, 2012). CPDs are the dominant by-products and have
Some physical nonthermal techniques do not inactivate caused the highest cytotoxic effects in microbial cells. On
microorganisms completely, thus resulted in sublethal the other hand, the 6–4 photoproducts exerted more lethal
injured microbial cells that can pose safety concerns due and mutagenic effects (Mitchell & Karentz, 1993).
to the ability of the microbes to regrow during storage or Meanwhile, UV light within the range of UVA wave-
transportation when a conducive environment is favorable length has the least influence on DNA due to its low
(Wu et al., 2020). UV light as a physical nonthermal tech- absorptivity in the DNA. Thus, it produced a negligible
nique has numerous mechanisms of action on living cells amount of CPDs (Jiang et al., 2009). However, UVA can
depending on its type and wavelength that target a specific still indirectly alter DNA by triggering photoreactions via
cellular component, thus causing some biological effects the generation of singlet oxygen (1 O2 ) (Alscher, Donahue,
(Yeo & Liong, 2012). As shown in Figure 2, DNA dam- & Cramer, 1997; Sinha & Häder, 2002). Nakahashi et al.
age is the primary biological effect observed in microbial (2014) revealed important changes in the DNA, including
cells after UV light exposure. Likewise, other biomolecules the production of 8-hydroxy-2′-deoxyguanosine (8-OHdG)
such as proteins and lipids experienced some form of bio- and CPDs as a result of lone UVA-LED and UVC irra-
logical defects due to the intense UV light. Proteins and diations, respectively. Similarly, Hamamoto et al. (2007)
lipids are viewed as the primary targets of reactive oxygen in their study reported the higher formation of 8-OHdG
species (ROS) produced by UV light, and this contributed in UVA-LED irradiated Salmonella enteritidis than that
to the indirect effect (Visser, Poos, Scheper, Boelen, & Duyl, recorded in UVC-irradiated bacteria at the same inactiva-
2002). tion level. The formation of these photoproducts inhibited
the normal replication and transcription of DNA, and thus
led to a mutation that resulted in the inactivation of the
2.1 DNA damage cells (Friedberb et al., 2006).

Among UV light-induced alteration in microorganisms,


the DNA damage brought on by UVC is the most signif- 2.2 Lipid oxidation
icant one. The UVC alteration involved the reactions of
adjacent thymines to form thymine dimers that result in UVA light is associated with ROS production and targets
changes in bioactive cell properties (Figure 2a). It is worth mostly the cellular membrane owing to its biomolecu-
noting that UV radiations (UVC and UVB) further gener- lar composition, mostly lipids. Besides the biomolecular
ate cyclobutane–pyrimidine dimers (CPDs) and 6–4 pho- composition, the presence of a large percentage of iron
3504 APPLICATION OF UV LEDS FOR INACTIVATION. . .

catalyzes the production of ROS generation. As depicted of the constraints related to UV-LEDs application. Some
in Figure 2b, the generated ROS has led to oxidation of studies were conducted to analyze the cost and forecast
fatty acids at lipid bilayer and pores formation, rearrange- the economic viability of UV-LEDs systems compared
ment of the phospholipid bilayer, and change of transmem- to conventional mercury lamps. Crook, Jefferson, Autin,
brane ion gradients (Kohen et al., 1995; Smith et al., 2009). MacAdam, and Nocker (2015) assessed the future eco-
The oxidative damage of the fatty acids also resulted in nomic cost of UV-LEDs systems in comparison to con-
the disruption of the cell membrane. The probable mod- ventional UV lamps. Their cost analysis was achieved by
ifications that occurred at the lipid bilayer level after the applying total expenditure (TOTEX) at two different disin-
UV radiations were a significant decline in membrane cov- fection levels of graywater. In both cases, the TOTEX cal-
erage with intact thickness and formation of hydrophilic culated over 15 years revealed that the UV-LEDs could not
channels in the membrane. Other notable modifications be qualified as an alternative to the traditional UV lamps
observed were loss of some lipid biomolecules and reor- due to their high economic cost. Nevertheless, it was pre-
ganization of the remaining lipids to form hemimicellar dicted that UV-LEDs would compete with conventional
edges of the hydrophilic channels (Smith et al., 2009). UV lamps in terms of cost by the year 2020. The economic
These findings showed that unsaturated fatty acids are viability of the UV-LED systems based on the whole life
more sensitive to UV light due to their structure (contains cost is expected to fall in 2020 (Ibrahim et al., 2014). Despite
double bonds) than the saturated lipids. their high cost in that period, UV-LED systems were pre-
ferred owing to their tremendous advantages, mainly being
environmentally friendly. The economic viability of LEDs
2.3 Protein alteration as a UV source for the application in AOPs was evalu-
ated by Autin et al. (2013). The study highlighted the eco-
In addition to DNA damage and lipid oxidation, protein nomic potential of the LEDs over the mercury lamps for
alteration also contributes to the inactivation of microor- the AOPs such as UV/TiO2 and UV/H2 O2 . This is because
ganisms by UV radiation (Visser et al., 2002). The appli- the price of the LEDs might drop from 210 to 0.05 £/bulb
cation of high UV light dose has detrimental effects on in a period extending from 2007 to 2020 (Ibrahim, 2012).
protein, such as the inhibition of critical cellular enzymes Recently, Taghipour (2018) reported that from 2019 to 2020,
function that lead to cellular dysfunction (Hoerter et al., UV-LEDs had dominated the disinfection and purification
2005). It has been demonstrated that UVA caused slacken- market due to their cost reduction.
ing protein synthesis as a result of tRNAs photo-damage To achieve the predicted cost-effectiveness, various tech-
(Oppezzo & Pizaorro, 2001). Meanwhile, the limited pen- nological parameters were developed by UV-LED man-
etration capacity and protein-induced damage of UVB is ufacturers, including power input, wall-plug efficiency,
small compared to UVC (Horikawa-miura et al., 2007). power output, and LEDs lifetime. The emergence of UV-
Despite this limited penetration, it results in extensive pro- LED systems dated back to the 2000s; in the beginning, the
tein damage and subsequent cell death. Santos et al. (2013) UV-LEDs were operating at lower power in the range of
assessed the UV light effect on protein conformational few milliwatts (Zhang et al., 2002). In the following years,
and compositional changes in Acinetobacter sp. and Pseu- the UV-LEDs input power was remarkably improved, and
domonas sp. using mid-infrared spectroscopy and sodium the output power was predicted to rise from 0.18 to 675 mW
dodecyl sulfate-polyacrylamide gel electrophoresis (SDS- from 2007 to 2020 (Ibrahim, 2012). Also, the wall-plug
PAGE). The results revealed critical changes in the protein efficiency was anticipated to reach 75% by 2020 (Song,
profiles of the two bacteria. Such changes were attributed Mohseni, & Taghipour, 2016).
to the oxidation of amino acids and other modifications on Currently, more advanced, energy, and cost-effective
biochemical processes such as propionylation, glycosyla- UV-LEDs are developed. Song, Taghipour, and Mohseni
tion, and phosphorylation. (2019) used three different LEDs of 265, 285, and 365 nm
wavelengths with a relatively high output power of 10, 30,
and 2,350 mW, respectively. Biancullo et al. (2019) used
3 UV-LED ADVANCEMENT FOR LEDs with a higher wavelength of 381 nm that possessed
MICROBIAL INACTIVATION a longer life span and intensity exceeding 70% after 10,000
hr of work. Similarly, 365-nm LEDs with a high power out-
The performance of the UV-LEDs has improved over the put of 1,613 mW and an efficiency of 12% were also reported
past decade with impressive performance regarding wall- (Lui, Roser, Corkish, Ashbolt, & Stuetz, 2016). Kim, Kim,
plug efficiency, LED input power, LED life, UV output and Kang (2017) utilized a UV-LED system made of four
power, and cost (Ibrahim, Macadam, Autin, & Jefferson, modules, and each one contained five LEDs of 279 nm
2014; Taghipour, 2018). High cost was reported to be one wavelength and a total of 200 mW power output. Other
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3505

types of UV-LEDs in the range of 265, 275, 310, and 365 nm ovirus type 2 (HAdV2), and Bacillus pumilus spores. All
wavelength, and power output of 1.1, 2.2, 1.3, and 6.8 mW, the UV sources performed almost similar inactivation of
respectively, were utilized with a current of 20 mA (Nyan- the microorganisms. The electrical efficiency of all the UV
garesi et al., 2019a). According to the data reported, the sources for microbial inactivation was estimated by eval-
longer the LED wavelengths, the more energy-efficient uating the electrical energy per order for E. coli and MS2
they are compared to the shorter wavelength LEDs. This is coliphage (EE0 ) (which is equivalent to the energy required
also similar to the lifespan, where 365- and 250-nm LEDs to decrease the concentration of the microorganism by
have a lifetime of 26,000 and 2,000 hr, respectively (Chen one order) and the energy required for 2-log reduction of
et al., 2017). HAdV2 (EEL.2 ). Contrary to other studies, the LP and MP
possessed the least EE0 of E. coli and MS2, compared to
260- and 280-nm UVC-LEDs. The LP and MP lamps also
4 COMPARISON OF UV-LEDS AND had the lowest EEL.2 for the inactivation of HAdV2. In this
CONVENTIONAL UV SYSTEMS FOR regard, it was suggested that in order to match the electrical
MICROBIAL INACTIVATION efficiencies (energy per log reduction) of conventional LP
UV sources, UVC LEDs must reach efficiencies of 25% to
Given the development of the UV-LED systems over the 39%.
last decades and their progressive domination in the dis- In a later study, Rattanakul and Oguma (2018) also
infection markets, UV-LEDs are considered as poten- investigated the electrical energy efficiency of 265, 280
tial competitors and alternative to the UV lamps. It is UVC-LEDs and 300 UVB-LEDs by evaluating the elec-
well established that UV-LEDs possessed more advan- trical energy required to inactivate 3 logs (EE,3 ) of all
tages over conventional lamps, including the low pres- the tested microorganisms, including E. coli, Bacillus sub-
sure (LP) and medium mercury (MP) lamps, being envi- tilis spores, Bacteriophage Qb, Legionella pneumophila, and
ronmentally friendly, and mercury-free. In terms of ger- Pseudomonas aeruginosa. Similar to the previous find-
micidal efficiency, numerous studies were conducted to ings by Beck et al. (2017), LP UV showed a better per-
compare the efficacy of UV-LEDs emission at different formance regarding electrical efficiency than all UV-LED
wavelengths with conventional lamps (Bowker, Sain, Shat- wavelengths based on the estimated EE,3 , which was the
alov, & Ducoste, 2011). lowest (0.006 to 0.064 kWh/m3 ). The variation in the EE,3 is
Li, Wang, Huo, Lu, and Hu (2017) compared both dis- related to the difference in wall-plug efficiency. Hence, the
infection efficiency and repair repression of E. coli using energy consumption needed for bacterial inactivation at a
two UVC-LEDs emitting at 265 and 280 nm with LP lamp specific level might be considered as an essential param-
(254 nm). The results showed that 265-nm UVC-LED had eter for a more reliable comparison between different UV
the best inactivation efficacy against E. coli compared to light sources.
280-nm UVC-LED and LP lamp. However, concerning Recently, a first full-scale UV-LED reactor, emitting light
photoreactivation and dark repair repression, the 280-nm at 275 nm, was utilized for the disinfection of drinking
UVC-LED treatment had a better effect than 265-nm UVC- water. This reactor was tested for bacteriophage (MS2)
LED and LP lamp as indicated by plate count and endonu- inactivation and then compared its effectiveness to con-
clease sensitive site (ESS) assays. Green et al. (2018) also ventional mercury UV reactors. The full-scale UV-LED
reported that at an equivalent dose of 7 mJ/cm2 for 259, and conventional mercury UV reactors had similar inac-
268, and 275 nm, UVC-LEDs recorded the same level of tivation performance. In order to improve the efficiency
inactivation or higher than LP lamps (253.7 nm) for E. coli, of the UV-LED reactors for a large-scale drinking water
Listeria, and Salmonella. Their selection of the wavelength disinfection, the power output, and the hydraulic profile
for achieving optimal treatment was based on the compari- must be improved (Jarvis, Autin, Goslan, & Hassard, 2019).
son of the different parameters of the LED wavelengths and
LP lamp, including the irradiance and germicidal efficacy.
These parameters were assumed to affect the treatment 5 INFLUENCE OF INDIVIDUAL
time, lifetime, and treatment cost. The study concluded UV-LEDS ON MICROBIAL INACTIVATION
that the 268-nm UVC-LED wavelength was the most effec-
tive. Therefore, it confirmed that the nearer the LED wave- LEDs have been proposed as alternative sources for the
length to 280 nm, the better the choice for effective UV- generation of UV light and may substitute conventional
LED performance. mercury lamps in the future (Kessler, 2013). The use of
On the other hand, Beck et al. (2017) compared 260 and LEDs provides a safe and efficient application of UV treat-
280-nm UVC-LEDs with LP and MP UV mercury vapor ment for water disinfection and food decontamination
lamps (254 nm) for E. coli, MS2 coliphage, human aden- without the risk of mercury contamination. LEDs are
3506 APPLICATION OF UV LEDS FOR INACTIVATION. . .

characterized by their ability to generate different ranges the inactivation of E. coli DH5, reaching a log survival ratio
of UV light, namely, UVA, UVB, and UVC. Consequently, of −3.23. Moreover, the study demonstrated that UVA-LED
UV-LED treatment can exert various effects, depending is appropriate for the treatment of fresh produce due to the
on the wavelength, bacteria strain, and disinfection media nonalteration in the quality attributes of the cabbage, such
used. Based on the available literature, UVC is the most as weight loss and vitamin C content (Aihara et al., 2014).
used for UV-LED treatment, as it was established to have Meanwhile, Haughton et al. (2012) investigated the appli-
the highest germicidal action. The influence and germici- cation of a near UV/visible 395 ± 5-nm LED for the decon-
dal actions of UVA-, UVB-, and UVC-LEDs are discussed tamination of raw chicken. Their results revealed reduc-
in the subsequent sections. tions of 2.21 and 2.62 log CFU/g in C. jejuni after 1 and 5 min
of treatment. In addition, the treatment did not affect the
color of the meat. Lian et al. (2010) employed 365-nm UVA-
5.1 UVA-LED LED for the inactivation of E. coli DH5α in colored bev-
erage, made from artificial pigments at different concen-
It has been established that UVA in the range of 365 nm trations. The aim was to assess the influence of the edible
wavelength posed a bactericidal effect with high penetra- pigments on the bactericidal action of the UVA-LED treat-
tion ability among the UV spectrum (Koutchma & Popović, ment. At UV dose of 126 × 103 mJ/cm2 , the reduction of
2019). Due to these essential characteristics of the UVA E. coli varied from 0.2 to 2 log CFU/mL depending on the
range, new UVA-LED setups were developed for water and type of the pigment and the concentrations used. The inac-
food disinfection (Mori et al., 2007). However, few stud- tivation of E. coli diminished at a higher concentration of
ies were carried out to assess the bactericidal action and the edible pigments (the inactivation of E. coli was greater
effectiveness of this UVA-LED, as presented in Table 1. in less concentrated solution). This could be explained by
Yagi et al. (2007) evaluated the effects of the application of the possibility of reflection that scattered the radiation.
UVA-LED treatment at a wavelength of 365 nm. The study Therefore, it is recommended to combine UV-LED treat-
proved the effectiveness of 365 nm wavelength of the UVA- ment with other sterilization methods to improve the inac-
LED to cause significant inactivation of both pathogenic tivation efficacy in liquid with a high absorption coef-
and nonpathogenic bacteria in phosphate-buffered saline ficient. UVA-LEDs have been recently employed for the
(PBS). The irradiation at UV doses of 9 × 106 and 27 × decontamination of low moisture foods. Pasard, Gänzle,
106 mJ/cm2 led to complete inactivation of Vibrio para- and Roopesh (2019) studied the potential of 365- and 395-
haemolyticus and E. coli, respectively. Whereas, the reduc- nm pulsed LEDs (UV dose: 0 to 834.4 × 103 mJ/cm2 and UV
tion rate of Salmonella reached 85% at 27 × 106 mJ/cm2 . intensity: 0.05, 0.23, 0.114, and 0.55 W/cm2 ) to inactivate
This indicated that sensitivity to UVA-LED varied based E. coli and S. enterica in both high (PBS) and low (dry bacte-
on the type of microorganism. Another study conducted ria) water activity (aw ) (aw = 0.75) media and dry pet foods.
by Hamamoto et al. (2007) showed that UVA-LED at a UVA pulsed-LED treatment at both wavelengths had a bet-
wavelength of 365 nm exerted a bactericidal effect on V. ter performance in the inactivation of bacteria suspended
parahaemolyticus, E. coli, S. enteritidis, and Staphylococ- in PBS (around 8 log CFU/g) than in dry bacteria (1 to 2 log
cus aureus in water. The treatment resulted in a reduc- CFU/g). A 365-nm pulsed-LED treatment was more effi-
tion higher than 5 log CFU/mL for all bacteria in less than cient than 395-nm pulsed LED in terms of energy input
75 min at 315 × 103 mJ/cm2 (excluding S. enteritidis with because 395-nm pulsed LED needed much higher dosage
log reduction >4 log CFU/mL within 160 min at 672 × than that of 365-nm pulsed LED to achieve the same inac-
103 mJ/cm2 ) which was less sensitive to UVA-LED treat- tivation level. Meanwhile, 395-nm pulsed LED at a dosage
ment. A recent study by Ahmed Malik et al. (2019) eval- of 658 × 103 mJ/cm2 was more efficient in the inactivation
uated the effectiveness of 385-nm UVA-LED against three of E. coli and S. enterica in pet foods (0.75%) compared to
pathogens, including S. aureus, P. aeruginosa, and E. coli 365-nm pulsed LED. Du, Prasad, Gänzle, and Roopesh
through measurement of inhibition zone after UVA-LED (2019) demonstrated in their study the potential of 395-
exposure at various times (1 to 60 min). Based on the nm UVA-LED in pulsed mode to inactivate Salmonella
inhibition zone diameters measurement, P. aeruginosa was ssp. in wheat flour in two different systems: open and
the most sensitive bacteria given its large inhibition zone semiclosed system. Wheat flour exposed to 395-nm UVA-
diameter (67 mm) followed by E. coli (55 mm) and S. aureus LEDs for 60 min led to a reduction of Salmonella by 2.42
(45 mm) as the most resistant bacteria to the UVA-LED and 2.91 log CFU/g in the open system and semiclosed
irradiation after 60 min exposure. system, respectively. Moreover, the functional and struc-
The effectiveness of UVA-LED treatment on surface tural changes of gluten have been also studied. The results
decontamination of solid food was investigated. Irradiation showed that exposure to 395-nm UVA-LED for 30 and
of cabbage tissues at 365 nm wavelength for 90 min led to 60 min triggered oxidation via generation of ROS that led to
TA B L E 1 Influence of UVA LED treatment on microbial inactivation in various media
Microorganisms Treatment media Treatment conditions Major findings References
V. parahaemolyticus, E. coli, S. Water λ: 365 nm ∙ 5 log CFU/mL reduction was obtained in V. (Hamamoto et al., 2007)
enteritidis, and S. aureus I: 70 mW/cm2 parahaemolyticus, E. coli, S. aureus, and E. coli DH5α.
D: 0 to 315 × 103 mJ/cm2 ∙ Inactivation of about 4 log CFU/mL was recorded in S.
APPLICATION OF UV LEDS FOR INACTIVATION. . .

t: 0 to 75 min enteritidis.

Candida albicans and E. coli phosphate-buffered Pulsed and continuous ∙ Pulsed irradiation had a greater germicidal effect than the (Li et al., 2010)
biofilms saline (PBS) exposure continuous irradiation mode.
λ: 365 nm.
I: 0.28 mW/cm2
pulses: 0 to 1,000 Hz
Duty rate: 25% to 75%

E. coli DH5α Colored beverage, λ: 365 nm ∙ UVA LED bacterial efficacy decreased with an increase in (Lian et al., 2010)
Orange juice I: 70 mW/cm2 the concentration of the pigments.
D: 126 × 103 mJ/cm2
t: 30 min

E. coli DH5α Cabbage, Lettuce λ: 365 nm ∙ Inactivation increases with the increase in exposure time. (Aihara et al., 2014)
I: 12.5 × 104 ∙ 90 min of the exposure led to 3.23 log CFU/g reduction.
mW/cm2
t: 0 to 90 min

Campylobacter jejuni and Raw chicken λ: 395 ± 5 nm ∙ Increase in inactivation with longer exposure times and (Haughton et al., 2012)
Campylobacter coli D: (0.06 to18) × 103 mJ/cm2 shorter distances from the UV source.
t: 30 s to 10 min ∙ No effect on the color of raw chicken.

(Continues)
3507
3508

TA B L E 1 (Continued)
Microorganisms Treatment media Treatment conditions Major findings References
S. aureus, P. aeruginosa, and Nutrient agar dish λ: 385 nm ∙ Pseudomonas aeruginosa was more sensitive to the UVA. (Ahmed Malik et al., 2019)
E. coli (solid media) t: 1 to 60 min ∙ The reduction rate of bacteria increased with the increase
in exposure time.

Salmonella spp. Wheat flour Pulsed UVA LEDs: ∙ An exposure time of 60 min induced reduction of (Du et al., 2019)
λ: 395 nm Salmonella by 2.42 and 2.91 log CFU/g in the open and
I: 0.45 W/cm2 semiclosed systems, respectively.
t: 0, 10, 30, 60 min ∙ The color of the flour was affected.
D: (270 to 1,620) × 103 mJ/cm2 ∙ No effect on rheological properties.
T◦ : 24 ◦ C (Open system) and
25 ◦ C (Semiclosed system).
RH: 42% (Open system) and
75% (Semiclosed system).

E. coli and S. enterica PBS Pulsed UVA-LEDs ∙ The inactivation efficacy depended on the dose, exposure (Pasard et al., 2019)
Pet foods λ: 365 and 395 nm time, aw, and bacterial strain.
I: 0.05, 0.23, 0.114, 0.55 W/cm2 ∙ Dry bacteria were more resistant to the treatment than
D: 0 to 834.4 × 103 J/cm2 the bacteria suspended in PBS.
High and low-aw conditions ∙ 365-nm LED was more effective than 395-nm LED for
inactivation of the pathogens suspended in PBS and dried
cells.
∙ 395-nm LED had a better performance than 365-nm LED
to inactivate the pathogens in pet foods.

Note. λ, wavelength; I, UV intensity; D, UV dose; t, treatment time; T, temperature.


APPLICATION OF UV LEDS FOR INACTIVATION. . .
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3509

TA B L E 2 Effect of UVB-LED treatment on microbial inactivation


Treatment Treatment
Microorganisms media conditions Major findings References
P. aeruginosa, L. Water λ: 300 nm ∙ E. coli was the most sensitive (Rattanakul &
pneumophila, E. coli, B. I: 1.01 mW/cm2 microorganism compared to the Oguma, 2018)
subtilis spores, and pathogenic bacteria and B. subtilis
bacteriophage Qb spores.

E. coli and Enterococcus Water λ: 310 nm ∙ UVB LEDs achieved about 5 log (Lui et al., 2016)
faecalis CFU/mL reduction within 3 hr of
treatment.

S. mutans, Streptococcus PBS λ: 310 nm ∙ UVB LED irradiation has a weak (Takada et al., 2017)
sauguinis, Porphyromonas I: 1.75 mW/cm2 bactericidal effect on oral bacteria.
gingivalis, and D: 17.5 to 265 mJ/cm2
Fusobacterium nucleatum
Pseudomonas aeruginosa Solid media λ: 296 nm ∙ UVB irradiation was effective for P. (Argyraki et al.,
biofilm D: 720 to 2 × 105 aeruginosa biofilms inactivation. 2016)
mJ/cm2 ∙ Higher resistance of mature P.
I: 1, 8, and 14 W/m2 aeruginosa biofilms
less than 15 min

Note. λ, wavelength; I, UV intensity; D, UV dose; t, treatment time; T, temperature.

bleaching of the wheat flour and polymerization of gluten tion was obtained at a UVB dosage of 2 × 105 mJ/cm2 .
proteins through disulphide linkage. In addition, the con- In contrast to the above study, Lui et al. (2016) men-
tent of the secondary conformation of gluten was modified tioned that 310-nm UVB-LED was less effective than other
by the increase of contents of intermolecular β-sheet and LED wavelengths used in the study (270 to 720 nm). The
β-turn structures. These modifications of gluten proteins irradiation by UVB-LED has only caused a reduction of
structure treatment might enhance the stability of gluten 1 log CFU/mL of E. coli and a negligible log reduction
network, therefore in terms of dough and bread making of Enterococcus faecalis. The weak bactericidal effect of
it might be beneficial for the mixing process and promot- UVB-LED was attributed to the low LED output power
ing the quality of the baking products. More studies are and the low sensitivity of the microorganisms. In related
required to explore the industrial feasibility UVA-LED sys- studies, Takada et al. (2017) observed that 310-nm UVB-
tems and their application for decontamination at different LED slightly inactivated oral bacteria, including Strep-
levels of food processing. tococcus mutans, Streptococcus sauguinis, Porphyromonas
gingivalis, and Fusobacterium nucleatum in PBS (less effi-
cient than UVC-LED treatment). The reduction rate of P.
5.2 UVB-LED gingivalis reached 47% to 58% in a time exceeding 30 s at
a UV dose of 52.5 mJ/cm2 . The F. nucleatum was reduced
UVB is another form of UV light utilized for medical to 53.5% after irradiation at 52.5 mJ/cm2 dose for 30 s, S.
purposes such as the treatment of infectious diseases sanguinis was reduced to 36% to 50% after 17.5 mJ/cm2
and sterilization of medical equipment (Argyraki et al., dose irradiation for 10 s, and S. mutans reduced to 52%
2016; Takada, Matsushita, Horioka, Furuichi, & Sumi, to 58% following a dose treatment of 17.5 to 420 mJ/cm2
2017). Table 2 outlined the key findings of UVB-LED stud- for 10 to 120 s. Rattanakul and Oguma (2018) compared
ies related to microorganism inactivation. Argyraki et al. three different LED wavelengths (265, 280, and 300 nm) for
(2016) compared the germicidal effect of 296-nm UVB- the inactivation of different microorganisms that included
LED and 266-nm UVC-LED on P. aeruginosa biofilms. vegetative cells of P. aeruginosa, L. pneumophila, and E.
The study revealed that the UVB-LED was more efficient coli, B. subtilis spores, and Bacteriophage Qb in water. The
than the UVC-LED in the inactivation of the biofilms. The results demonstrated that K values (maximum inactiva-
UVB-LED irradiation completely inactivated the P. aerug- tion rate constant, cm2 /mJ) at 300 nm wavelength for veg-
inosa biofilms grown for 24 hr at a dosage of 105 mJ/cm2 etative bacteria, spores, and bacteriophage QB were low-
against a 1 log CFU/mL reduction for UVC LED irradia- est among other wavelengths. The low K values indicated
tion at the same dose. Meanwhile, for the fully matured the low sensitivity of these microorganisms to the 300-nm
biofilms (grown for 72 hr), only 3.9 log CFU/mL reduc- LED, and hence, depicted inadequacy of the wavelength
3510 APPLICATION OF UV LEDS FOR INACTIVATION. . .

for such microorganisms’ inactivation. Further studies are lengths. Also, when energy efficiency is taken into consid-
needed to assess the applicability of UVB-LEDs for food eration, still the pulsed mode resulted in a better perfor-
decontamination. mance compared to the continuous mode. Zhou, Li, Lan,
Yan, and Zhu (2017) reported that the US pretreatment
has positively affected UV-LED inactivation on E. coli in
5.3 UVC-LED deionized water (DI), DI containing kaoline suspension
(DIK), and secondary effluent (SE) of municipal wastew-
UVC range is the most used among other UV-LED cat- ater treatment plant. A better inactivation rate constant
egories for decontamination due to its high germicidal was observed when the samples were pretreated with US
action. Table 3 highlights some applications of UVC-LED (40 s, 66 W/L) followed by UVC-LED radiation (254 nm,
treatments in various media. UVC-LEDs are mainly used 0 to 30 mJ/cm2 ). An improved inactivation from 0.24 to
for the disinfection and purification of drinking water and 1.07 log CFU/mL for each dose was recorded in DIK, while
wastewater to substitute chlorination. This is to ensure an increase of 0.07 to 0.55 log CFU/mL was noticed for
consumers’ safety and prevent environmental contamina- each dose in SE. It was hypothesized that the US pretreat-
tion by harmful chemical components (Chevremont, Far- ment attenuated the shielding effects caused by the pres-
net, Coulomb, & Boudenne, 2012; Gross, Stangl, Hoenes, ence of suspended particles in turbid liquids. US pretreat-
Sift, & Hessling, 2015; Vilhunen, Särkkä, & Sillanpää, 2009; ment reduced photoreactivation, thus promoted disinfec-
Würtele et al., 2011). Chatterley and Linden (2010) eval- tion efficiency (Zhou et al., 2017). UVC-LEDs have been
uated the germicidal effect of 265-nm LED wavelength employed to control microbial contamination in the food
for the inactivation of E. coli in water. The irradiance of industry to address food safety concerns. Murashita, Kawa-
20 mJ/cm2 led to 3.3 log CFU/mL reduction of E. coli. mura, and Koseki (2017) studied the potential of UVC-
Crook et al. (2015) employed a 255-nm UV-LED source LED (270 to 280 nm) to reduce nonpathogenic E. coli
with varying doses of 0 to 120 mJ/cm2 for graywater treat- ATCC 25922, E. coli O157: H7, S. enterica Typhimurium,
ment. At UV dose of 41 mJ/cm2 , the irradiation resulted and L. monocytogenes in ice cubes. The results revealed
in a total inactivation of E. coli and Enterococci, whereas that UVC-LED at a dosage of 15.2 mJ/cm2 led to a 4.45
120 mJ/cm2 dose achieved a reduction of 5 log CFU/mL log CFU/mL reduction of E. coli ATCC 25922. L. monocy-
for total coliforms. In this study, the presence of particles togenes was the most sensitive among the pathogen as it
has affected the disinfection efficacy. The treatment was was completely inactivated at 40 mJ/cm2 . However, E. coli
more efficient in the graywater with smaller particles than O157: H7 and S. enterica Typhimurium required a higher
that with large ones. This could be attributed to the parti- dose of 160 mJ/cm2 to achieve 6 to 7 log cycles reduc-
cles shielding effect on the microbial cells during the UV tion. Kim and Kang (2020a) applied the UVC-LED at a
radiation. Similarly, Nelson, McMartin, Yost, Runtz, and wavelength of 280 nm at doses varying from 0 to 21.6
Ono (2013) reported that UV radiation was less effective mJ/cm2 for inactivation of E. coli O157: H7 S. Typhimurium,
in reducing coliform bacteria in wastewater because of the and L. monocytogenes in different media surfaces includ-
high turbidity. ing selective media, deli meat, and spinach. Their results
Shin, Kim, Kim, and Kang (2016) used UVC-LED to demonstrated that UVC-LED was more effective on E. coli
inactivate various microorganisms on solid media, includ- inactivation in selective media surface. It required 1.35 s
ing E. coli, Salmonella typhimurium, and Listeria mono- (2.2 mJ/cm2 ) and 3.60 s (5.9 mJ/cm2 ) to reach 3 log reduc-
cytogenes. They found that the exposure to the 275-nm tions of E. coli and S. Typhimurium, respectively, whereas
LED at a dose of 1.61 mJ/cm2 led to a 5 to 6 log CFU/mL L. monocytogenes required more than 4.5 s (9.3 mJ/cm2 ).
reduction for E. coli and S. typhimiurium, while over 5 log For sliced meat, a dose of 21.6 mJ/cm2 achieved 1.0 to 1.6 log
CFU/mL reduction was observed for L. monocytogenes at reductions of the three pathogens. Similar to the selective
the same dose. The inactivation rate of the bacteria was media, L. monocytogenes was the most resistant among the
increased with the increase in temperature and UV-LED pathogens. For spinach, a dosage of 21.6 mJ/cm2 recorded
dosage. In this type of treatment, the potency of the UVC 2.4 to 2.6 log reductions of the three pathogens. In another
can be enhanced by pulse mode application. A recent study study, UVC LED treatment was applied to decontaminate
by Zou et al. (2019) buttressed this point. The researchers low water activity foods such as wheat flour. A 275-nm
compared the efficacy of 265- and 280-nm LEDs in a contin- pulsed LED at a dose of 60.1 mJ/cm2 and an intensity of
uous and pulsed mode for E. coli inactivation. The results 16.7 µW/cm2 for 60 min achieved 1.07 log/CFU reduction
revealed that the pulsed treatment achieved a better inac- of Salmonella with no color changes in the treated wheat
tivation. A decrease in the duty cycle from 100% to 5% flour (Subedi, Du, Prasad, Yadav, & Roopesh, 2020). UVC-
(an essential parameter in pulsed UV-LED treatment) led LED treatments have also been utilized for the decontam-
to the decrease of E. coli inactivation under both wave- ination of various contact surfaces during food processing.
TA B L E 3 Influence of different UVC-LED treatments on microbial inactivation
Microorganism Treatment media Treatment conditions Major findings References
Escherichia coli O157: H7, Solid media and water λ: 275 nm ∙ Increased irradiation dosage and temperature resulted in 5 to 6 (Shin et al., 2016)
Salmonella Typhimurium, and I: 5.57 µW/cm2 log CFU/mL reductions of E. coli O157: H7 and S.
Listeria monocytogenes. T: 0 to 5 min Typhimurium.
T: 0 to 37 ◦ C ∙ A 5 log CFU/mL for L. monocytogenes was recorded at a dose of
1.67 mJ/cm2 .

E. coli, bacteriophages MS-2, and PBS λ: 255 and 275 nm ∙ The wavelength of 275-nm LEDs had a better bactericidal effect (Bowker et al., 2011)
T7 I: 0.046 to 0.11 µW/cm2 than 255 nm for T7 and E. coli.
t: 0 to 1,577 s ∙ The wavelengths of 255- and 275-nm UV-LEDs produced
comparable microbial inactivation for MS-2.
APPLICATION OF UV LEDS FOR INACTIVATION. . .

E. coli water λ: 265 nm ∙ An irradiance of 20 mJ/cm2 led to 3.3 log CFU/mL reduction of (Chatterley & Linden,
D: 0 to 20 mJ/cm2 E. coli. 2010)

E. coli Water λ: 265 and 280 nm in continuous ∙ High current pulsed irradiation of 280 nm LEDs wavelength (Zou et al., 2019)
and pulsed mode achieved better inactivation than 265 nm wavelength.
t: 1 to 20 min
D: 8.4 mJ/cm2

E. coli water λ: 250, 265, and 280 nm ∙ 1.0 and 2.5 log CFU/mL E. coli reductions in water following 20 (Nelson et al., 2013)
t: 20 to 50 min and 50 min of UV-LED exposure, respectively.
∙ UV was less effective in reducing coliform bacteria in
wastewater.

E. coli Deionized water (DI), DI λ: 254 nm ∙ U.S. pretreatment significantly improved the UVC LED (Zhou et al., 2017)
water with kaoline D: 0 to 30 mJ/cm2 irradiation efficacy.
suspension (DIK), and US pretreatment: 40 s, 66 W/L
secondary effluent (SE)
E. coli, Enterococci, and Graywater λ: 255 nm ∙ UVC LED efficiently inactivated all bacteria. (Crook et al., 2015)
Total coliforms D: 0 to 120 mJ/cm2 ∙ Suspended particle sizes influenced disinfection efficiency.

E. coli, S. aureus, L. Peptone water λ: 266 to 279 nm ∙ Inactivation rate was enhanced with an increase in the UV (Kim et al., 2017)
monocytogenes, Saccharomyces D: 0.1 to 0.6 mJ/cm2 dose.
pastorianus, and Pichia ∙ Distinct microorganisms showed different sensitivities to the
membranaefaciens UV-LED treatments.

E. coli O157: H, S. enterica serovar Sliced cheese λ: 266 to 279 nm ∙ Short peak LED wavelengths (266, 270 nm) had better (Kim, Kim, & Kang,
Typhimurium, and L. D: 1 to 3 mJ/cm2 inactivation compared to the long peak wavelengths (275 to 2016)
monocytogenes 279 nm).
∙ No changes in the color of the cheese.

(Continues)
3511
TA B L E 3 (Continued)
3512

Microorganism Treatment media Treatment conditions Major findings References


E. coli ATCC 25922, E. coli O157: Ice cubes λ: 270 to 280 nm ∙ UVC-LED efficiently inactivated nonpathogenic E. coli. (Murashita et al., 2017)
H7, S. Typhimurium, and L. T◦ : -30 ◦ C ∙ L. monocytogenes was the most sensitive among all pathogens.
monocytogenes. I: 0.005 to 0.0085 mW/cm2 ∙ L. monocytogenes required a lower dose for the total
D: 0 to 160 mJ/cm2 inactivation compared to E. coli O157: H7 and S. Typhimurium.

E. coli O157: H7, S. Typhimurium, Selective media λ: 280 nm ∙ E. coli was the most sensitive to the treatment in selective (Kim & Kang, 2020a)
and L. monocytogenes. Sliced deli meat D: 0 to 21.6 mJ/cm2 media.
Spinach ∙ E. coli was completely inactivated at an exposure time of 1.35 s,
while S. Typhimurium and L. monocytogenes required much
longer treatment times.
∙ UVC- LED treatment was less effective in the inactivation of
pathogens in sliced deli meat and spinach surfaces compared
to selective media.

E. coli O157: H7 S. Typhimurium, Food contact surfaces: UVC LED: ∙ UVC-LED fulfilled 0.5 to 1 log reductions of foodborne (Kim & Kang, 2020b)
and L. monocytogenes Glass, PVC, Stainless λ: 280 nm pathogens depending on the surface characteristics.
steel (SUS), Teflon, and D: 0.5 to 3 mJ/cm2 ∙ The bactericidal effect decreased in this order: glass, PVC, SUS,
silicon. UVC LED + mild heat: Teflon, and silicon.
λ: 280 nm ∙ UVC-LED + mild heat resulted in an additive or synergistic
T◦ : 60 ◦ C effect on the inactivation of the three microorganisms.
D: 0.5 to 3 mJ/cm2

Salmonella and E. coli Coriander UVC LED: ∙ The UVC-LED treatment resulted in 0.4 to 1.3 log CFU/g (Jiang, Ai, Liao, Liu, &
λ: 280 nm Salmonella and E. coli reductions, varying with the exposure Ding, 2020)
I: 80, 160, 240 µW/cm2 time and the irradiation intensity.
Slightly acidic electrolyzed water ∙ E. coli was more resistant to UVC-LED treatment than
(SAEW)/UVC-LED: Salmonella.
ACC (SAEW): 20, 40, 60 ppm ∙ SAEW/UVC-LED combined treatment could improve the
T (SAEW): 1, 3, 5 min bactericidal efficiency of microorganisms on the surface of
I: 80, 160, and 240 µW/cm2 coriander leaves.
t (UVC LED): 5, 15, and 30 min ∙ SAEW/UVC-LED treatment did not alter overall coriander
quality.
∙ SAEW/UVC extended the shelf-life of coriander.

Salmonella Wheat flour Pulsed UVC LED: ∙ Reductions in Salmonella cell counts of 1.07 after 60 min at 25 (Subedi et al., 2020)

λ: 275 nm C and an RH of 75%.
I: 16.7 µW/cm2 ∙ No color changes in the wheat flour.
D: 60.1 mJ/cm2
Relative humidity (RH): 40%,
75%, and 90%.

Note. λ, wavelength; I, UV intensity; D, UV dose; t, treatment time; T, temperature.


APPLICATION OF UV LEDS FOR INACTIVATION. . .
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3513

FIGURE 3 Main effects of combined different UV light wavelengths treatment

Kim and Kang (2020b) reported in their study that UVC- coli reduction. Moreover, sensory evaluation and storage
LED at a wavelength of 280 nm at a varying dose of 0.5 to tests demonstrated that UVC-LED/SAEW contributed to
3 mJ/cm2 .The treatment led to 0.9 to 1.44, 0.5 to 1.66, the quality preservation (color, texture, and smell) and
and 0.5 to 0.91 log reductions of E. coli O157: H7, S. extension of shelf life of the coriander. This contradicted
Typhimurium, and L. monocytogenes, respectively, on var- the study of Martin et al. (2016) in which UV LED treat-
ious food contact surfaces: glass, PVC, stainless steel, ment negatively influenced sensory quality of fluid milk
Teflon, and silicon. The inactivation efficacy depended after 4 h of exposure. In general, UV LED has shown
on the surface characteristics such as hydrophobicity and its effectiveness against the proliferation of some impor-
roughness. UVC-LED had the greatest performance when tant food pathogens of great concern in the food sector.
applied on glass, and the inactivation efficacy decreased However, some sensory quality changes reported in some
in PVC followed by stainless steel, Teflon, and silicon. To food products such as liquid milk require the attention of
enhance the UVC-LED performance, UVC-LED treatment food researchers and processors. Therefore, more in-depth
was simultaneously combined to 60 ◦ C mild heat. A syn- investigation of food quality toward consumer perception
ergistic bactericidal effect was observed on L. monocyto- should be prioritized since consumer liking is affected.
genes (̴ 2 log reductions). Whereas, an additive effect was
observed for E. coli O157: H7 and S. Typhimurium (Kim &
Kang, 2020b). In a recent study conducted by Jiang et al. 6 COMBINATION OF DIFFERENT
(2009), UVC-LED treatment was combined with slightly UV-LEDS AT VARIOUS WAVELENGTHS
acidic electrolyzed water (SAEW) to enhance the decon- FOR TREATMENT OF MICROORGANISMS
tamination efficacy of Salmonella ssp. and E. coli in corian-
der. The SAEW pretreatment of coriander at various ACC 6.1 Effect of combined UV-LEDs
(20, 40, 60 ppm) followed by 280-nm UVC-LED at a UV wavelength on microbial inactivation
intensity of 80, 160, 240 µW/cm2 for 5, 15, 30 min. The
results revealed that the combined SAEW/UVC-LED treat- A combination of different UV-LED wavelengths has been
ment at UV dosage of 240 µW/cm2 for 30 and 5 min suggested as a hurdle approach for enhancing microbial
washing in SAEW (ACC of 60 ppm) induced 2.72 log decontamination efficacy (Figure 3a) (Chevremont et al.,
CFU/g Salmonella reduction and 2.42 log 7 2 CFU/g E. 2012; Nakahashi et al., 2014b). In this context, such treat-
3514 APPLICATION OF UV LEDS FOR INACTIVATION. . .

ment applied either simultaneously and/or sequentially iphage inactivation, without consideration of simultane-
has resulted in additive, antagonistic, or synergistic effects ous or sequential exposures or UVA exposure time (Song
(Berdejo, Pagán, García-Gonzalo, & Pagán, 2019). Recent et al., 2019). Multiple wavelengths combination of 260/280-
studies conducted on the effect of combined UV-LEDs nm LEDs (simultaneous application) did not have synergy
wavelength for the treatment of microorganisms are sum- on HAdV2, MS2 coliphage, and B. pumilus spores inac-
marized in Table 4. tivation nor for genetic material alteration (DNA level).
Recent findings by Green et al. (2018) revealed that the However, the treatment had synergy for E. coli inactiva-
simultaneous application of combined 259/289-nm UV- tion (Beck et al., 2017). Nyangaresi et al. (2018) established
LEDs treatment at a UV dose of 14 mJ/cm2 synergistically no synergistic effect from the application of UVC/UVC
reduced E. coli and Listeria seeligeri count by 2.42 and 4.87 (267/275 nm), UVC/UVA (267/310 nm), and UVC/UVA
log CFU/mL reduction, respectively. Xiao, Chu, He, Liu, (275/310 nm) LEDs combinations on E. coli inactivation
and Hu (2018) demonstrated that the sequential applica- during water disinfection. Akgün and Ünlütürk (2017)
tion of UVA-LEDs and UVC-LEDs amplified the inactiva- observed no synergistic effect on the reduction of E. coli
tion of E. coli ATCC 11229, E. coli ATCC 15597, and E. coli during a combined treatment of different UV-LEDs wave-
ATCC 700891 by 1.3, 0.9, and 0.5 logs CFU/mL, respec- lengths in two types of apple juices. The UV-LED irradi-
tively. According to the researchers, the preradiation with ation exerted a better inactivation on the clear apple juice
UVA made the three strains less resistant to UVC-LEDs. than the cloudy one. This was linked to the low penetration
The inactivation of E. coli ATCC 25922 by UVC-LEDs was capacity of UV radiation in liquid food with a high absorp-
decreased after UVA exposure. Even though UVA radi- tion coefficient. The combination of UVA and UVC LEDs
ation did not cause a direct effect, its introduction has exhibited better preservation of the color of the cloudy
either negatively or positively affected the UVC resistance apple juice compared to the individual UVC LED and
of the four strains. In another study, a synergistic effect thermal treatments. The combined treatment also raised
was observed when 254/365-nm UV-LEDs were applied on polyphenol oxidase inactivation to 67.42% and 65.62%
V. parahaemolyticus compared to the effect of the indi- for 280/365 and 280/405-nm LEDs’ wavelengths, respec-
vidual LEDs (Nakahashi et al., 2014). Also, the combined tively. However, more studies are needed to understand
treatment of 254/365-nm UV-LEDs at UV dose 4.9 mJ/cm2 the synergistic effects on both microbial inactivation and
and 280/365-nm UV-LEDs at 5.59 mJ/cm2 on mesophilic quality.
bacteria in wastewater resulted in 2.1 and 3.5 log CFU/mL
reduction after 30 min. The inactivation result was higher
than that obtained with the individual UV-LEDs treat- 6.2 Effect of combined UV-LED
ments at the same doses (Chevremont et al., 2012). Qiao, wavelengths on bacterial reactivation:
Chen, and Wen (2018) found that a combined 280/350-nm photo and dark repair
UV-LEDs induced synergistic bactericidal effect on sapro-
phytic bacteria at UV fluence of 51 µW/cm2 . Rantalankila, Many researchers have claimed the ability of some
Koivistoinen, Sarvasidze, and Sillanpää (2016) reported microorganisms, particularly bacteria, to reactivate via
the UV treatment under sequential 274 + 278-nm UV- repairing their DNA damage after exposure to UV light. To
LEDs resulted in the greatest inactivation of Asterionellop- counteract the destructive effects of DNA lesions, a mech-
sis glacialis. anism of DNA repair is mainly photoreactivation and exci-
Based on these reports, not all multiple UV-LEDs wave- sion repair (dark repair) taking place within the microbial
lengths combination result in synergistic effects. Simul- cells. This phenomenon is considered one of the significant
taneous and sequential exposures to 265-nm UVC-LED drawbacks of UV treatment as it decreases its efficiency. To
(4.2 mJ/cm2 ) and 285-nm UVB-LED (15.3 mJ/cm2 ) did overcome this problem, multiple UV wavelength combina-
not induce any synergistic effect. Instead, the treatment tions were suggested and have been tested on numerous
resulted in an additive effect of 4.6 log CFU/mL inacti- microorganisms (Chevremont, Farnet, Sergent, Coulomb,
vation of E. coli irrespective of the succession order of & Boudenne, 2012).
UVC-LEDs and UVB-LEDs application. This could be
attributed to the similar damage effects caused by UVB
and UVC radiations (photochemical reaction) at the DNA 6.2.1 Photoreactivation
level of the microorganisms. Likewise, the application of
UVA-LEDs (365 nm) followed by UVB-LEDs (285 nm) or Photoreactivation is regarded as one of the most straight-
UVC-LEDs (265 nm) showed a synergistic effect on the forward repair paths. An enzyme called photolyase
inactivation of E. coli. However, an additive effect was catalyzes this process, and the mechanism of action of
noticed when similar wavelengths were used for MS2 col- this enzyme consisted of binding the main photoproducts
TA B L E 4 Effects of combined UV-LED wavelengths treatment on microorganisms
Disinfection
Wavelengths (nm) Microorganism media Treatment condition Major findings References
UVC-LEDs: 259, 268, and E. coli, Salmonella, Listeria Saline solution UV dose: 7 mJ/cm2 ∙ Inactivation above 3 and 4 log CFU/mL depending on (Nyangaresi et al.,
275 nm seeligeri UV dose (259/289): 14 the UV dose and wavelength. 2018)
UVB: 289 nm mJ/cm2 ∙ 267 nm had the highest inactivation efficiency.

UVA: 370 nm UVC/UVB: T : 4 ◦ C and 25 ◦ C ∙ Photoeffect was the dominant mechanism of
259/289 nm, reactivation.
UVC/UVA: 259/370 nm. ∙ No synergistic effect for combined wavelengths
APPLICATION OF UV LEDS FOR INACTIVATION. . .

Low pressure mercury (UVB/UVC).


lamp (LPM): 253.7 nm ∙ Electrical energy consumption was lower for the 275-nm
UV-LED

UVC: 267 & 275 nm E. coli Water UV dose: 8.78 to 23.04 ∙ 268 and 259 nm achieved the highest log count (Green et al., 2018)
UVA: 310 nm mJ/cm2 reduction on all strains
UVC/UVC: 267/275 nm ∙ 259/289 had a synergistic effect on reduction of E. coli
UVC/UVA: 267/310 (2,42 ± 0,31) and λ Listeria (4,87 ± 0,07) yielding 1.6 to
UVC/UVA: 275/310 0.6 log higher reduction
∙ UV-LEDS in the 259 to 275 have shown more effective
than LPM
∙ UV-LED treatment was effective at refrigeration
temperatures

UVA LED pretreatment E. coli ATCC 11229, E. coli Water Sequential radiation of ∙ 20 min UVA preradiation resulted in the inactivation of (Xiao et al., 2018)
followed by UVC-LED: ATCC 15597, E. coli 365 UVA (20 to E. coli ATCC 11229, E. coli ATCC 15597, E. coli
365 + 265 ATCC700891, E. coli 30 min) 265 and UVC ATCC700891 by 1.2, 1.4, and 1.2 times, respectively.
ATCC 25922 (5 to 16 min). ∙ 20 min UVA radiation had higher inactivation rates on
Light intensity three strains than the sum of inactivation rates by UVA
I(UVA) = 6 mW/cm2 alone and UVC alone.
I(UVC) = ∙ Enhancement of CPD induced by UVC radiation after
0.127 mW/cm2 UVA preradiation.
∙ Inhibition of dark repair capacity.
∙ No changes in the photo repair capabilities for all
strains.
(Continues)
3515
3516

TA B L E 4 (Continued)
Disinfection
Wavelengths (nm) Microorganism media Treatment condition Major findings References
E. coli K12 (ATCC 25253) Clear apple juice 2 (Akgün &
UVC: 254 UV dose: 707.2 mJ/cm ∙ Highest inactivation (2 log reduction) of E. coli K12 for
UVC: 280 Cloudy apple Exposure time: 20 to CAJ when treated for 40 min at 280 and 280/365 nm. Ünlütürk, 2017)
UVC/UVA: 254/365 juice 40 min. ∙ AJ achieved a 4.4 when exposed to 280-nm LED for
UVC/UVA: 254/405 40 min.
UVC/UVA: 280/365 ∙ In cloudy apple juice at 280 to 365 nm at 40 min of
UVB/UVA:280/405 exposure time resulted in 3.9 and 2 log CFU/mL in clear
UVC/UVB/UVA/UVA: and cloudy apple juices.
254/280/365/405 ∙ UVC/UVA LEDs combination had a synergistic effect on
the reduction of PPO activity (to 32.8% CAJ).

LEDs: E. coli Water UV dose (mJ/cm2 : ∙ 265 nm was more effective than 280-nm LEDs and LP (Li et al., 2017)
UVC: 265, UVB: 280, UVC: 10.91 UV lamps.
UVC/UVB: 265/280 UVB:15.35 ∙ No synergistic effect for disinfection from the
(50%), UVC/UVB: (50%): 12.57 combination of 265 and 280 nm.
UVC/UVB: 265/280(75%) UVC/UVB (75%): 13.78 ∙ 280 nm could repress photoreactivation and dark repair.
Low pressure (LP) UV LP UV lamp: 13.03
lamp: 265

LEDs E. coli Water T◦ : 22 ◦ C ∙ UVC/UVB had an additive effect on microorganism (Song et al., 2019)
UVC: 265, UVB: 285, UVA: Coliphage MS2 UV exposure time: 40 s inactivation for both microorganisms.
365 for E. coli and 3 min ∙ UVA pretreatment followed by UVC improved E. coli
UVC/UVB: 265/285 for MS2 inactivation.
UVB/UVA: 285/365 UV dose: ∙ Additive effect on MS2 was observed under various
UVC/UVA: 265/365 UVC-LED: 4.2 mJ/cm2 wavelength combinations.
UVB-LED: 15.3 mJ/cm2
UVA-LED: 1,160
mJ/cm2

LEDs: Saprophytic bacteria, Iron Subsea oil-field UV fluence:51µW/cm2 ∙ Combined 280 and 350 nm induced synergistic (Qiao et al., 2018)
UVC: 255 bacteria, injection bactericidal effects on saprophytic bacteria.
UVB: 280 Sulfate-reducing bacteria water ∙ 280 nm resulted in high performance in both energy
UVC/UVA: 255/350 efficiency and reactivation suppression
UVB/UVA: 280/350
(Continues)
APPLICATION OF UV LEDS FOR INACTIVATION. . .
TA B L E 4 (Continued)
Disinfection
Wavelengths (nm) Microorganism media Treatment condition Major findings References
LEDs: ∙ E. coli K12 (ATCC29425) Water Irradiance ∙ E. coli: all five sources attained over 3 -log reduction at (Beck et al., 2017)
UVC: 260, UVB: 280 ∙ MS2 coliphage (ATCC 0.19 to 0.55 mW/cm2 UV doses of 12 mJ/cm2 .
UVC/UVB: 260/280 15597-B1) UVC LED ∙ MS2 coliphage: 260 nm 280-nm LEDs achieved 2- log
MP ∙ Human adenovirus type 0.35 to1.17 mW/cm2 for inactivation at a UV dose of 30.3 and 38.5 mJ/cm2 ,
LP 2 HAdV2 the MP UV respectively, and 32.8 mJ/cm2 for the combined
∙ B. pumilus spores 0.3 to 0.75 mW/cm2 for 260/280 nm LEDs.
the LP UV ∙ Adenovirus: 4-log reduction at 122, 89, and 105 mJ/cm2
for the 260, 280, and 260 to 280-nm LEDs, respectively.
APPLICATION OF UV LEDS FOR INACTIVATION. . .

∙ B. pumilus spores: 260 and 260/280-nm UV irradiation


were more effective than the 280-nm UV irradiation for
2-log reduction.
∙ No dual-wavelength synergies were detected for
bacterial and viral inactivation nor DNA and RNA
damage.

LEDs: Asterionellopsis glacialis Seawater Dose-based treatment ∙ Dose-based efficiency evaluation did not present any (Rantalankila et al.,
UVC: 265, 262, 268, (100 to 2,000 mJ/cm2 ) clear distinction between different wavelength LEDs. 2016)
274, 278 Time-based ∙ The best time-based performance in the inactivation
UVC/UVC: 256 + 262, treatment(1/min) rate was observed using 274 and 278-nm LED with an
262 + 268, 268 + 274, 274 + inactivation rate constant of 0.1296 1/min.
278

LEDs: Vibrio parahaemolyticus Water UV intensity: 700 ∙ Increase of DNA product 8-hydroxy-2′-deoxyguanosine (Nakahashi et al.,
UVA: 365, UVC: 254 RIMD2210633 W/m2 (8-OHdG) after UVA irradiation alone and cyclobutane 2014b)
UVA/UVC: 365/254 pyrimidine dimers (CPDs) after UVC irradiation alone.
∙ Additional effect induced by sequential irradiation with
UVA-LED and UVC-LED.
∙ Simultaneous irradiation with UVA-LED and
UVC-induced bactericidal synergistic effects due to
suppression of CPDs repair.

LEDs: E. coli (ATCC 11303, ATCC Wastewater pH: 6 and 8 ∙ The 280/365 or 280/405 nm coupled wavelengths, had (Chevremont et al.,
280, 365, 405 15597, and CIP 6224) Exposure time: 60, 120, the most important bactericidal effect. 2012)
254/365,254/405, 280/365, Enterococcus faecalis and 180 s ∙ Absence of bacterial reactivation after 60 s of exposure
280/405 (ATCC 19433 and ATCC to UV.
33186)
3517
3518 APPLICATION OF UV LEDS FOR INACTIVATION. . .

(CPD photolyase or 6–4 photolyase) that are at the ori- UV by generating ROS (Almeida & Sobol, 2007). Simi-
gin of DNA damage. This process occurs during exposure lar to photoreactivation, the inhibitory effect of the dark
to the visible/blue light (330 to 480 nm) via reversing the repair of E. coli was highest at wavelength 280 nm (Li et al.,
alteration caused by UV light at the DNA level (Essen & 2017). Nyangaresi et al. (2018) found that 275-nm UV-LEDs
Klar, 2006; Kim, Heelis, & Sanear, 1992). A recent study wavelength exerted the lowest dark repair compared to the
demonstrated that photoreactivation is the most important combinations of 265 nm (UVC-LED), 275/310 nm (UVC/
mechanism of reactivation that occurred during UV-LED UVA-LEDs), and 265/275 nm (UVC/UVC-LEDs). This
treatment of E. coli in water treatment. After processing emphasized the vital role of 275 nm wavelength on pro-
with different dual combination of different wavelengths tein damage. It has been suggested that combining UVC
of UVA/UVC-LEDs (310/275 nm) and UVC/UVC-LEDs treatment with UVA reduced the occurrence of dark
(267/275 nm) treatment, the photoreactivation was signif- repair (Figure 3b). This suggestion was supported by Xiao
icantly repressed compared to those of 267-nm UV-LED. et al. (2018), in which it was revealed that the UVA
The single treatment resulted in the highest inactivation as (pretreatment)-UVC system inhibited dark repair capac-
against the combinations of 310/275 nm (UVA/UVC-LEDs) ity for four E. coli strains. The simultaneous application of
and 267/275 nm (UVC/UVC-LEDs). This might be due to UVA-LED (365 nm) and UVC/UVB LEDs (265/285 nm) or
the crucial role of the wavelength of 275 nm in repress- sequential combination of UVA (365 nm) and UVC/UVB
ing photoreactivation through protein damage (Nyan- LEDs (265/285 nm) reduced the inactivation of E. coli
garesi et al., 2018). Qiao et al. (2018) reported that simul- due to persistence of photoreactivation and dark repair.
taneous combined UV-LED wavelengths of 280/365 nm However, extending the UVA-LED pretreatment followed
(UVC/UVA-LEDs) suppressed the reactivation of sapro- by UVC-LED improved the E. coli inactivation efficacy
phytic bacteria. This was due to the inclusion of 280 nm by suppressing the dark repair process (Song et al.,
wavelength or wavelengths close to 275 nm that helped to 2019).
repress photoreactivation. A similar assertion was made in
the inactivation of E. coli when a wavelength of 280 nm
repressed the photoreactivation of the bacteria (Li, Wang, 7 UV-LEDS AND AOPs
Huo, Lu, & Hu, 2017). However, the photo repair capac-
ity of E. coli ATCC 11229, ATCC 15597, ATCC 700891, To promote UV treatment efficacy, many researchers sug-
and ATCC 25922 remained stable after the application gested the combination of UV light with a wide range of
of a sequential combination of UVA (365 nm) and UVC catalysts including H2 O2 , TiO2 , O3 , Fe (VI), ZnO2 , and
(265 nm) LEDs. This was probably related to the UVA dose ZnS to accelerate the generation of reactive radicals when
utilized (108 × 106 J/cm2 ) used for the treatment that only exposed to the adequate wavelength, this process is known
induced sublethal damage (Xiao et al., 2018). According to as AOPs (Fang et al., 2014; Jung, Oh, & Kang, 2008; Wu
Webb (1977), UVA preradiation required UV doses exceed- et al., 2017). AOPs have been used as alternatives to conven-
ing 750 × 106 J/cm2 in order to achieve the reduction of tional treatment of drinking water and wastewater, such as
the photo repair process by means of the ROS generation. chlorination and ozonation advanced filtration processes
In other words, DNA damage as a result of exposure to and germicidal ultraviolet (UV) radiation (Bhatkhande,
high doses of UV light has caused an irreversible DNA Pangarkar, & Beenackers, 2002). Conventionally, AOPs are
deterioration as the photons generated by UV acts rapidly performed using low or medium pressure mercury lamps
within the irradiated cells (Beggs, 2002) due to the inhi- as UV light source. However, these sources have their dis-
bition of crucial enzyme photolyase as demonstrated in advantages (Wang et al., 2012). Recently, UV-LED technol-
Figure 3b. Therefore, to minimize the photoreactivation, ogy was introduced to perform the AOPs due to its advan-
it is suggested that the UV dose should be increased to tages. Several studies have explored the applicability of
counter such an effect. UV-LED-based AOPs and the effects on both photocatal-
ysis inactivation of bacteria and micropollutants removal
(Eskandarian, Choi, Fazli, & Rasoulifard, 2016; Kuipers,
6.2.2 Dark repair Bruning, Yntema, & Rijnaarts, 2015). AOPs have proved to
be useful for both microbial disinfection (bacteria spores
In contrast to photoreactivation, excision repair is com- and viruses) and degradation of micropollutants such as
prised of multiple steps. First is the dark repair pathway, dye, pharmaceuticals, and phenol (Benabbou, Derriche,
which is further divided into two subpathways, namely, Felix, Lejeune, & Guillard, 2007; Kabra, Chaudhary, &
base excision repair (BER) and nucleotide excision repair Sawhney, 2004; Mamane, Shemer, & Linden, 2007; Pablos,
(NER) (Rastogi, Kumar, Tyagi, & Sinha, 2010). BER is the Marugán, van Grieken, & Serrano, 2013; Vilhunen & Sil-
principal DNA repair pathway originated by the indirect lanpää, 2009).
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3519

FIGURE 4 Principle and effect AOPs microbial inactivation and degradation of organic pollutants

The mechanism of photocatalytic bacterial inactivation most explored AOPs is UVA-LED/TiO2 because of their
induced by AOPs has been discussed by Dalrymple et al. chemical stability, nontoxicity of TiO2 , and its effectiveness
(2010). It can be observed that ROS generated during the under near-ultraviolet light (300 to 400 nm) (Markowska-
AOPs target different cell components, mainly cell mem- Szczupak, Ulfig, & Morawski, 2011; Wu, Xie, Imlay, &
branes, cell walls, and peroxidation of proteins, polysac- Shang, 2009). This range of wavelength is less expensive
charides, lipopolysaccharides, peptidoglycan, and phos- than the UVC range and requires small energy, and there-
pholipid as shown in Figure 4. Other effects of AOPs were fore, has a longer lifetime. In AOPs, longer UV wavelengths
the oxidation of nucleic acids and the destruction of the are preferred than the short ones due to their ability to
enzymes and coenzymes. Upon attack by AOPs, the cells excite the photocatalysts and produce ROS (Province et al.,
undergo lysis leading to cell death. Likewise, the mech- 2011). Table 5 summarized related studies of UV-LEDs-
anism of micropollutants degradation was proposed in based AOPs for microorganisms inactivation. Province
Figure 4, and involved the complete breakdown of the pol- et al. (2011) used two UVA-LED wavelengths of 370 and
lutants to harmless components such as carbon dioxide or 377 nm combined with 0.01% of TiO2 for the inactivation
ions such as nitrates, sulfate, and chloride. The mineral- of B. subtilis in PBS. It was found that 370-nm LED/TiO2
ization of the pollutants, depending on their nature and was more efficient than the extended treatment using a
composition to harmless substances, were also established wavelength of 377-nm LED. It required less than 100 min
(Carrier et al., 2006; Jo & Tayade, 2014). at UV-LED power of 3 mW for complete inactivation of B.
subtilis, whereas 377 nm wavelength reduced B. subtilis to
7.1 Effects of UV-LEDs-based AOPs on less than 1 log CFU/mL at the same exposure and UV-LED
microorganism inactivation power. In another study, Biancullo et al. (2019) showed that
the addition of TiO2 at a concentration of 100 g/L during
In order to select an effective UV-LED-based AOPs for the UV-LED treatment at 381 nm led to a decrease of 2 log
decontamination, the inactivation efficiency, reactivation, CFU/mL for heterotrophs, enterococci, and E. coli in urban
ability to repair suppression, and the economic aspect wastewater. Some bacteria might exhibit some resistance
related to energy consumption are considered. One of the to such treatment. Province et al. (2011) reported regrowth
TA B L E 5 Summary of the studies that have been conducted on UV-LED-based AOPs for disinfection and micropollutant removal in water
3520

Microorganisms/Micropollutants Disinfection media Treatment conditions Major findings References


E. coli ATCC 700891 Water UVA LED/TiO2 ∙ Enhancement of the inactivation of E. coli with the (Xiong & Hu,
λ: 365 nm increase of UV light intensity 2013)
I: 6 to 8 mW/cm2
TiO2 film (73 ± 0.5 mg)

Bacillus subtilis PBS UVA LED/TiO2 ∙ The time required for complete inactivation of B (Province et al.,
λ: 370 and 377 nm .subtilis by UV-LED/TiO2 is 2011)
C (TiO2 ): 0.01% wavelength-dependent.
∙ 370-nm LED was more efficient than a longer
wavelength of 377-nm LED.

E. coli, heterotrophs, and enterococci Urban wastewater UVA LED/TiO2 ∙ Decrease of the bacterial load by 2 log-units. (Biancullo et al.,
λ: 381 nm 2019)
C (TiO2 ): 100 g/L

B. subtilis spores Water UVC LED/Chlorine ∙ Combined UV-LED with chlorine induced (Li et al., 2018)
λ: 265 and 280 nm synergistic effect on B. subtilis spores inactivation.
D: 125 mJ/cm2 ∙ The efficiency of the treatment depended on the
C (Cl2 ): 4 mg/L UV-LED wavelength and the pH of chlorine.

E. coli Urban wastewater Photocatalytic ozonation ∙ Photocatalytic ozonation was efficient for (Moreira et al.,
Enterobacter cloacae Drinking water O3 /UVA LED/TiO2 microorganisms and antibiotic resistant genes 2016)
Achromobacter sp. λ: 382 nm (ARGs) removal.
Enterococcus faecalis

Escherichia, Citrobacter, Enterobacter, and Raw river water UVA LED/TiO2 ∙ The combination of UVA LED with different (Claro et al., 2016)
Klebsiella UVA LED/SiZnO, N-SiZnO, photocatalysts performed a high inactivation
and F-N-SiZnO. efficiency exceeding 95%.
I: 580 mW/cm2
λ:385 nm
t = 0 to 60 min
concentration of the
photocatalyst: 0.5 g/L

E. coli Water UV-LEDs/TiO2 : ∙ Increasing the irradiance enhanced the (Nyangaresi et al.,
λ: 265, 275, 310, and 365 nm inactivation of E. coli in both photolysis (UV-LED) 2019b)
I: 0.49 mW/cm2 and photocatalysis (UV-LED/TiO2 ).
C(TiO2 ): 0 to 0.1 g/L ∙ 275 nm combined with TiO2 was more effective for
both inactivation and repair suppression and
required lower energy consumption.

Note. λ, wavelength; I, UV intensity; D, UV dose; t, treatment time; T, Temperature; C, concentration of the photocatalyst.
APPLICATION OF UV LEDS FOR INACTIVATION. . .
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3521

of heterotrophic bacteria following after storage at room at a concentration of 1 g/L reduced the bacterial load
temperature in the dark for 3 days. of E. coli, enterococci, and heterotrophs and their antibi-
Claro, Bidoia, and de Moraes (2016) assessed the hetero- otics resistant group to about 2 log CFU/100 mL. The bac-
geneous photocatalysis using a UVA-LED as a source of terial regrowth was observed for total heterotrophs and
UV light in the presence of three synthesized photocata- their antibiotics groups, after the storage of photocatalytic
lysts SiZnO, N-SiZnO, and F-N-SiZnO. The photocatalytic treated wastewater. Some of the microorganisms remained
inactivation efficiency of the three catalysts was then com- viable and regrew during the storage. Hence, the evalua-
pared to TiO2 added at a concentration of 0.5 g/L. The tion of the probable regrowth after AOPs treatment or the
combined treatment of the UVA-LED and the three pho- residual disinfecting effect could be beneficial for an ade-
tocatalysts were effective against coliforms yielding 95% of quate selection of UV dose and wavelength to avoid the
inactivation. This corresponded to the efficiency of the reactivation. This aspect should be considered in the future
UVA-LED/TiO2 . Nyangaresi et al. (2019b) employed four design of energy-efficient setups for AOPs.
different LED wavelengths (265, 275, 310, and 365 nm) com-
bined with TiO2 for the inactivation of E. coli in water. They
found that an increase in irradiance positively affected the 7.2 Degradation of micropollutants by
efficiency of photocatalysis. Meanwhile, 275-nm LED com- UV-LEDs-based AOPs
bined with 1 g/L of TiO2 was preferred among the other
UV-LED-based AOPs in terms of inactivation efficiency, The presence of organic contaminants in water or wastew-
suppression of repair, and energy consumption. Li et al. ater and their degradation is considered as a major
(2018) investigated the inactivation of B. subtilis spores in challenge, due to the high resistance of the organic
water, using a combination of UV-LEDs emitting at 265 pollutants to treatments such as ozonation, chlorination,
and 280 nm at a UV dose of 125 mJ/cm2 and chlorine filtration, coagulation and, UV light treatment (Legrini,
(Cl2 ) of 4 mg/L concentration. The combined treatment Oliveros, & Braun, 1993; Vieno, Härkki, Tuhkanen, &
resulted in a synergetic effect with log reductions of 1.8 Kronberg, 2007). To overcome this limitation, UV-based
and 1.5 log CFU/mL for UV265 /cl2 and UV280 /cl2 , respec- AOPs were exploited as a novel strategies to degrade these
tively. These log reductions were two times higher than pollutants (Pablos et al., 2013; Qin et al., 2014; Xiang, Fang,
those obtained during lone treatments of UV 265 and 280- & Shang, 2016). Likewise, UV-LEDs have been used to
nm LEDs and Cl2 . The study further emphasized the con- substitute conventional mercury lamps as a source of UV
tribution of ROS such as OH⋅ in the inactivation of the radiation (Autin et al., 2013; Kuipers et al., 2015). Many
spores. Xiong and Hu (2013) submitted water to combined studies have demonstrated the potential of UV-LEDs-
UVA-LED (365 nm) and TiO2 biofilm at UV fluence ranged based AOPs for the degradation of a wide range of organic
from 6 to 8 mW/cm2 to assess the inactivation and reac- pollutants. The recent advances in the application of LEDs
tivation of antibiotic resistance E. coli ATCC 700891. The for the degradation of organic contaminants based on
treatment was effective against the E. coli, with a reduction AOPs have been studied elsewhere (Matafonova & Batoev,
of 3 log CFU/mL observed after the combined treatment. 2018). Among UV-LEDs-based AOPs that are utilized, UV-
The study further analyzed the residual disinfection effect LEDs/chlorine and UV-LEDs/TiO2 for the degradation of
at different periodic time of 30, 60, and 90 min. The resid- pharmaceutical residues such as carbamazepine (CBZ),
ual disinfecting effect was significant with periodic illumi- acetaminophen (ACT), diclofenac (DCF), ibuprofen
nation of 30 min, while residual disinfecting effect could (IBP), sulfamethoxazole (SMX), azithromycin, trimetho-
inactivate almost all the total bacteria after 90 min UV peri- prim, and ofloxacin (Biancullo et al., 2019; Eskandarian
odic illumination. et al., 2016; Wang et al., 2017). The UV-LEDs/TiO2 treat-
Moreira et al. (2016) focused on the effect of photo- ment of urban wastewater has reduced azithromycin,
catalytic ozonation (O3 /UVA-LED/TiO2 ) on enterococci, trimethoprim, ofloxacin, and SMX antibiotics to values
enterobacteria, fungi, and antibiotic-resistant bacteria below the detection limits and to decrease the bacte-
(ARB) and their resistant genes (ARGs) in treatment of rial count by 2 log CFU/mL after 1 hr. Although the
urban wastewater and surface drinking water. The photo- antibiotics were effectively oxidized by UV-LEDs/TiO2
catalytic ozonation exhibited an intense germicidal action, photocatalysis, microbial regrowth was observed after
thus reduced the ARGs to very low levels in the urban storing the treated wastewater for 3 days (Biancullo
wastewater and surface water. Moreover, the microbial et al., 2019). Similarly, UV-LEDs/TiO2 photocatalysis
regrowth of the ARGs after treatment remained stable was responsible for the decomposition of ACT, DCF,
during 3 days of storage at room temperature. Another IBP, and SMX in wastewater. The degradation followed
study conducted by Biancullo et al. (2019) demonstrated the order SMX > DCF > IBP > ACT, and shorter UV
that UV-LEDs at wavelength 381 nm combined with TiO2 wavelength in the sequence UVC- > UVB- > UVA-LED
3522 APPLICATION OF UV LEDS FOR INACTIVATION. . .

was more potent during the degradation. The mineral- which have drastically reduced the economic cost. This
ization of these pharmaceuticals also corresponded to progression has made UV-LEDs at the forefront concern-
the trends observed for their disappearance (Eskandarian ing the disinfection, purification, and decontamination
et al., 2016). The degradation of CBZ in wastewater by UV- in environmental (wastewater and municipal drinking
LED/chlorine oxidation was studied. At 280- and 310-nm water) and food industries as an alternative for the tradi-
UV-LED/chlorine irradiation, efficient degradation of CBZ tional UV lamps. The combination of different UV-LED
was achieved, and the degradation rate was onefold higher wavelengths as hurdle strategies due to their synergistic
in magnitude than that obtained with UV-LED/H2 O2 effects on microbial inactivation and reactivation suppres-
treatment. The generated ROS such as OH and Cl radicals sion has exponentially advanced. These hurdle approaches
accounted for more than 80% of the CBZ decomposition at depended on the treatment conditions, including wave-
neutral conditions during the UV-LED/chlorine treatment lengths and the order of application (sequential or simulta-
(Wang et al., 2017). UV/H2 O2 system for the photodegra- neous), disinfection media, UV dose, type of microorgan-
dation of aqueous phenol using different wavelengths of isms used (vegetative and spores forming bacteria or virus),
255, 265, and 280 nm, viewing angle and H2 O2 concen- and the strain. The probable synergism of the various com-
trations were investigated. The degradation of the phenol bined UV-LEDs wavelengths concerning microbial inacti-
was observed to be most efficient with 280-nm UV-LED vation, reducing treatment time, and energy consumption
wavelength due to its highest optical power (Vilhunen & were elucidated. Moreover, the application of UV-LEDs
Sillanpää, 2009). for AOPs for photocatalysis inactivation of bacteria and
On the other hand, UV-LEDs/Photo-Fenton process was degradation of micropollutants in water were discussed.
tested for the removal of pesticide acetamiprid. High- The UV-LEDs-based AOPs depended on several factors,
intensity UV-LED system effectively degraded acetamiprid including intensity, wavelength, UV-LED type, the concen-
pesticide after 20 min at natural pH with sequential addi- tration of chemical oxidizers, and molecular structures of
tion of 1 + 1 + 1 mg Fe/L (iron dosage) and 12 mg H2 O2 /L. micropollutants.
It was hypothesized that both H2 O2 and Fe have equal More investigations are needed for both combined UV-
contribution to the formation of ROS radicals in the UV- LEDs for food preservation to elucidate their influence
LED system (Carra et al., 2015). Further applications of on the food quality attributes, interaction with bioactive
AOPs in the treatment of wastewater from food process- food components, and consumer acceptance. UV light was
ing industries such as olive mill, winery, meat, poultry, and reported to trigger flavor deterioration, which might result
dairy have been extensively reviewed elsewhere (Amor, in the formation of secondary metabolites, thus leading to
Marchão, Lucas, & Peres, 2019; Krzemińska, Neczaj, & negative consumer liking. Such an assertion should be fur-
Borowski, 2015). Based on these studies, UV-LEDs-based ther investigated to ascertain the safety of UV LED-treated
AOPs have potentials in the treatment of water utilized foods. UV-LED-based AOPs for microbial inactivation in
in the processing of foods and wastewater generated from agricultural food products need to be further exploited.
the processing chain to simultaneously achieve microbial Also, UV-LEDs hurdled with other physical nonthermal
inactivation and degradation of the organic pollutants. technologies, or natural antimicrobials should be exploited
The effectiveness of the UV-LEDs-based AOPs depends at food safety level.
on the intensity, wavelength, UV-LED type, chemical con-
centration of oxidizers, and molecular structures. There- AC K N OW L E D G M E N T S
fore, the development of higher intensity UV-LEDs could The authors acknowledge Conselho Nacional de Desen-
lead to more feasible economically viable technological volvimento Científico e Tecnológico (CNPq, Grants
options capable of satisfying the microbial and pollu- #302763/2014-7 and #305804/2017-0) and the Coordenação
tant elimination requirements concerning food and water de Aperfeiçoamento de Pessoal de Nível Superior - Brasil
safety. (CAPES) - Finance Code 001 for the financial support.

8 CONCLUSION CONFLICTS OF INTEREST


The authors declare no conflict of interest.
UV-LED treatment is a potential nonthermal technology
utilized over the past decade for water disinfection and AU T H O R CO N T R I B U T I O N S
food decontamination. UVA-, UVB-, and UVC-LEDs have Yasmine Kebbi and Aliyu Idris Muhammad drafted the
successfully reduced microbial loads, mainly in water, liq- manuscript. Tian Ding and Anderson S. Sant’Ana crit-
uid, and solid foods. Over the years, UV-LED reactors have ically revised the article. Leonardo do Prado-Silva and
undergone significant changes regarding wall-plug effi- Donghong Liu conceptualized the idea and drafted the
ciency, input and output power, and a lifetime of the LEDs, outline.
APPLICATION OF UV LEDS FOR INACTIVATION. . . 3523

ORCID Berdejo, D., Pagán, E., García-Gonzalo, D., & Pagán, R. (2019).
Aliyu Idris Muhammad https://orcid.org/0000-0002- Exploiting the synergism among physical and chemical processes
1788-3482 for improving food safety. Current Opinion in Food Science, 30, 14–
20. https://doi.org/10.1016/j.cofs.2018.08.004
Donghong Liu https://orcid.org/0000-0003-0028-232X
Bhatkhande, D. S., Pangarkar, V. G., & Beenackers, A. A. C. M. (2002).
Tian Ding https://orcid.org/0000-0002-8403-5344
Photocatalytic degradation for environmental applications—A
review. Journal of Chemical Technology and Biotechnology, 77(1),
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