Electrochemical (EC) disinfection of water and wastewater has been widely mentioned  - . Numerous pathways have been proposed to explain the EC action, including: 1) oxidative stress and cell loss of life due to electrochemically formed oxidants, 2) irreversible permeabilization of cell membranes by the applied electric field (EF), 3) and electrooxidation (EO) of vital cellular constituents during exposure to electric current or induced EFs  - .
While EF is applied on water carrying microorganisms with plunged electrodes, chemical oxidants are generated      . Electrolysis forms numerous oxidants in the occurrence of oxygen (O2), comprising hydrogen peroxide (H2O2) and ozone (O3), as well as free chlorine (Cl2) and chlorine dioxide (ClO2) when chloride ions (Cl−) are existing in water    . Such oxidants are mostly accountable for the deadliness of the applied direct current (DC) . Numerous scientists established the synergetic contribution of antimicrobial agents and EF in neutralizing pathogens   - .
EFs are naturally fatal to cells. This is mainly attributed to the irreversible permeabilization of the cell membrane   . Through experiments realized on artificial bi-film lipid membranes it was proved that a membrane exposed to an outer EF collects charge much like a capacitor, and a transmembrane potential is produced . A short-lived steady-state current across the membrane is initiated when the membrane is completely loaded, showing an induced permeability of the membrane to hydrophilic molecules. Such a phenomenon is largely explained by models involving the formation of transient pores in the membrane due to the application of the outer EF. The reversibility of such an electro-permeabilization is influenced by two key factors: The level of the formed transmembrane potential, and the period of application of the outer EF. For cells, transmembrane potentials over 1 V and longer pulse times lead to irreversible permeabilization and cell dying. The transmembrane potential produced by an outer EF is a function of the size of the cell membrane, with bigger cells experiencing a bigger transmembrane potential from an applied EF. As a result, the level of the field required to kill yeast cells is frequently smaller than that requested to neutralize microbes . Death takes place due to either the apparition of constant pores and following destabilization of the cell membrane or mislaying of crucial cell constituents and demolition of chemical gradients via transport across transient pores . If formed oxidants by EC techniques are existing, these pores could authorize the oxidants open entrance to the inside of the cell, contributing to the demobilization phenomena    .
EFs possess as well the capability of demolishing cells in the absence of demolishing their membranes. Matsunaga et al.  explained a technique in which cells were eliminated in the absence of breaking, only a little with the EO of intracellular coenzyme A  . Consequently, EFs can straight oxidize cellular compounds, leading to cell dying    .
Several researches have been dedicated to the employ of EFs and currents to eliminate bacteria and yeast in industrial and medical applications, as indicated by the next cases. Potable water polluted with Escherichia coli (E. coli) K12 (100 cells/cm3) was disinfected at a rate of 600 cells/cm3/h with the use of a 0.7 V electric potential using a carbon cloth electrode . Potable water polluted with 335 cells/mL total coliforms and 1035 cells/mL fecal streptococci was sterilized with a 2.5 mA/cm2 DC density (125 mA current) applied with 5 cm × 5 cm titanium electrodes for 30 min . DC (60 mA) was employed to impede the development of E. coli, Bacillus subtilis, Pseudomonas aeruginosa (P. aeruginosa), and Staphylococcus aureus contaminants of a bioprocess reactor . Grahl and Markl  focused on a non-thermal pasteurization technique that can avert to touch the vitamins, enzymes, texture, and taste of treated foods. They followed the impact of pulsed EFs on E. coli and Saccharomyces cerevisiae suspended in milk and fruit juice, respectively . Bacteriophages stay alive short applications to different current magnitudes in an EC cell better than bacteria at both low (1 × 103 colony-forming units (CFUs)/mL) and high (1 × 106 CFUs/mL) population density . Electrolyzed water had been found to possess an elevated lethal performance than Ca(OCl)2 of the alike measured active Cl2 dose . During the treating time, fundamentally internal cell constituents of the microorganisms enter in chemical reactions with the disinfectants  - .
Regardless of the reality that the deactivation of bacteria by different EC disinfection means has been reported in the literature, the influence of process variables and reactor conception on kill performance remain to be fully understood. Further, a small number of researches focused on the mechanisms of EC disinfection. This review concentrates on EC microbial killing mechanisms. Several related and pertinent references are examined and key EC mechanisms are discussed. The effect of electrode material on the pathogens’ killing is discussed. The EC disinfection is compared with other methods in terms of performance in neutralizing microbes. Free radicals’ contribution to killing pathogenic microorganisms and the EF impact are reviewed. Finally, propositions for better EC disinfection especially in terms of DBPs control are presented.
2. Influence of Electrode Material on the Microbial Demobilization
The nature of electrodes has a key role in electrocoagulation (ECG) process. Ghernaout et al.  used ordinary steel, stainless steel (SS), and aluminum electrodes. Ordinary steel (U = 12 V) and aluminum (U = 11.8 V) give to the solution Fe2+(aq) and Fe3+(aq) (neutral pH) and Al3+(aq), respectively; however, SS (U = 10.7 V) does not produce any metallic ions to the solution. Reduction of cellular concentration at 620 nm as a function of electrode nature is shown in Figure 1. For the first 10 min (Figure 1), SS (55.45%) is less efficient than ordinary steel
Figure 1. Reduction of cellular concentration of E. coli as a function of electrodes nature during electrocoagulation (ECG) (I = 1 A) .
(97.18%), which is less than aluminum (98.16%). These results may be explained by the fact that all bacteria are not eliminated or demobilized; a portion of the bacteria may be absorbed on flocs generated during ECG using Al or Fe electrodes  .
Jeong et al.  studied the action of electrode material on the formation of oxidants, and illustrated the various reaction mechanisms for forming individual oxidants by using boron-doped diamond (BDD), Ti/RuO2, Ti/IrO2, Ti/Pt?IrO2, and Pt as anode materials. The performance of hydroxyl radical (●OH) generation was in the arrangement of BDD >> Ti/RuO2 ≈ Pt. No crucial formation of ●OH was detected at Ti/IrO2 and Ti/Pt?IrO2. The ●OH was proved to have a fundamental contribution in O3 formation at BDD, but not at the other electrodes. The generation of active Cl2 was in the arrangement of Ti/IrO2 > Ti/RuO2 > Ti/Pt?IrO2 > BDD > Pt. The great gap in this arrangement, from that of reactive oxygen species (ROSs), was assigned to the divergence in the electrocatalytic activity of each electrode material with regard to the formation of active Cl2.
Similar results were achieved by López-Gálvez et al. . Table 1 presents the important mechanisms proposed explaining the deadliness of EC technique and their respective cited references.
3. Electrochemical (EC) Control of Bacterial Persister Cells
The appearance of antibiotic-resistant bacteria has given an augmenting defiance to infection monitoring . Classical techniques of antibacterial remediation including elevated dose of antibiotics or surgical intervention have been shown inadequate for eliminating constant infections, such as those linked with medical implants. It is well established that bacterial populations frequently hold a low percentage of phenotypic variants, called persister cells, which are metabolically idle and very resistant to antibiotics. When the antibiotic remediation is ceased, remaining alive persister cells may revive the bacterial population with a comparable percentage of persister cells. Therefore, pertinacity gives a hard defiance to curing chronic infections. Niepa  presented a new technique for monitoring bacterial pertinacity founded upon a process which was called EC control of
Table 1. Main mechanisms suggested interpreting the deadliness of EC treatment and their cited references.
persister cells. This researcher  proved that bacterial persister cells could be efficaciously removed by low-level DC; as an example, remediation with 70 μA/cm2 DC for 1 h utilizing SS 304 decreased the number of viable planktonic persister cells of P. aeruginosa PAO1 by 98% in comparison with the untreated control . DC applications have an effect on surface charge and membrane integrity of P. aeruginosa, conducting to augment intracellular concentration of metal cations . In addition, EC treatments interposed via carbon electrodes induced the permeabilization of the cells to extracellular materials, and elevated their sensibility to antibiotics, which conducted to total elimination of the persisters .
4. Technology Efficiency: Electrochemical (EC) Disinfection vs. Other Methods
The EC technique was greatly efficient for wastewater remediation . An E. coli eliminating performance of 100% may be obtained for the model water with a residence time of only 0.5 min and a current density (CD) of 25 mA/cm2 (Table 2). While the CD was decreased to 16 mA/cm2, a residence time of 2 min was required to give a disinfection performance of 99.98%. EC disinfection was much more performant than classical chlorination. A residence time of at least 30 min was needed for chlorination to reach a bactericidal performance of 99.94% or greater. EC disinfection seemed to possess a germicidal performance even bigger than ozonation in terms of residence period. The Fenton reaction was not illustrated as the most efficient disinfection techniques for the model water; however, this was probably formed by the low dosage of Fenton’s reagent used in the experimental tests in comparison with the most Fenton reaction conditions.
Diao et al.  concluded that all of the disinfection techniques studied in their research (i.e., EC disinfection, chlorination, ozonation and the Fenton reaction), were powerful in eliminating E. coli with an initial density of 108/mL in the examined wastewater. With an eliminating performance of 99.4% or greater, almost all of the cells in the disinfected samples lost their viability from the viewpoint of being biologically available to incubation (Figure 2).
5. Electrochemical (EC) Disinfection Mechanisms
In a general manner, the deactivation of bacteria during disinfection operation
Figure 2. Scanning electron microscopy (SEM) photographs of E. coli cells in (a) fresh culture and after (b) chlorination at 5 mg/L for 30 min; (c) ozonation at 10 mg/L for 5 min; (d) the Fenton reaction with 8.5 mg/L H2O2 and 0.85 mg/L Fe2+ at pH 4 for 10 min; (e) EC disinfection at 16 mA/cm2 for 2 min and (f) EC disinfection at 25 mA/cm2 for 2 min .
Table 2. Experimental conditions and bactericidal performances of various disinfection techniques .
may be usually interpreted by two kinds of destruction to bacterial cells . Primarily, disinfectants may enter in reaction with cell area constituents inducing cell membrane permeability variations or the malfunction of enzymatic diffusion procedures. Secondly, damages to the intracellular constituents, particularly the loss of DNA integrity, may be generated with or without evident cell area destructions . Some disinfectants produce more important deteriorations to either the cell surface area or interior constituents; however, these two kinds of deteriorations are not limited, depending on the Ct value (disinfectant dose × residence time) and kind of bacterial cells. While EC disinfection, the behavior of E. coli and Enterococcus is very various, particularly at the start of the process if the concentration of oxidants was less than 2 mg/L (0 - 5 min, 4 V) . Comparable findings were observed in the survey on classical chlorination disinfection treatment . The various deactivation kinetics enter the two indicator bacteria are probably linked to their cell surface structure variations (Gram-negative vs. Gram-positive bacteria), because at low Cl2 concentration (<0.5 mg/L, as Cl2), deteriorations of Cl2 were detected importantly to the cell areas . When the Cl2 dose overpass the minimum (1.5 ≤ Cl2 ≤ 3 mg/L), hard deteriorations to bacterial genomes may appear  .
Lacasa et al.  concluded that the main inactivation mechanisms involve 1) mechanical stress (only for Artemia salina), 2) direct oxidation on the surface of conductive diamond anode, and 3) chemical reactions with chlorine species and/or ROSs (●OH, O3 or H2O2).
6. Electrochemical (EC) Disinfection’s Free Radicals: Key Contribution in the Killing Actions
As mentioned previously, the elevated performance of EC disinfection may be given by short-lived and energy rich intermediate products with a more efficient killing capacity . These chemical products obviously comprise free radicals (e.g., ●OH− and O2●−)     . By their SEM examination (Figure 2), Diao et al.  presented more proof of the hypothesis concerning the important contribution of ●OH− in EC disinfection. Cell samples disinfected by ●OH− of the Fenton reaction had a rather comparable look as those after EC remediation. There was crucial degeneration and decomposition of the cells following from both the Fenton reaction and EC disinfection. Liberated cellular materials were collected on the filters, which was remarkable to a lesser amplitude for the samples of ozonation and narrowly remarkable for the samples of chlorination. Consequently, in addition to electro-chlorination, E. coli cells during EC remediation were probably deactivated by the intermediate products with an oxidizing strength comparable to that of free radicals and much powerful than that of Cl2 .
Bio-electro-Fenton devices have been adopted as a cost-efficient and highly efficacious water treatment technique . Zhou et al.  studied the demobilization of E. coli in a microbial electrolysis cell-based bio-electro-Fenton system (microbial electrolytic-Fenton cell). They proved that a 4-log reduction of E. coli (107 to hundreds CFUs/mL) was attained with an externally applied voltage of 0.2 V, 0.3 mM Fe2+, and cathodic pH of 3.0. Nonetheless, insignificant demobilization was noted in the control tests without external voltage or Fe2+ dose. The killing impact was improved when the cathode airflow rate augmented from 7 to 41 mL/min and was also in proportion to the elevation of Fe2+ level from 0.15 to 0.45 mmol/mL. Fatal cell membrane destruction by ●OH was considered as one possible pathway for neutralizing pathogens.
7. Suggestions for Better Electrochemical (EC) Disinfection
The real possibilities of the performant disinfection given with the electro-chlorination technique, as an example of EC disinfection, are various. Because disinfection practically may perform with a single pass, the application of the process is very simple in comparison with chemical oxygen demand (COD) elimination, in which recirculation or some type of cascade procedure with several cells has to be utilized. Experience has practically been reached utilizing in-line electro-chlorination for remediation and disinfection of salt water swimming pools, in which the ameliorated disinfection performance from the passing of the cells lets it easy to function at much lower residual Cl2 concentrations (<0.2 mg/L) that again reduces the concentrations of disinfection by-products (DBPs)  .
Tanaka et al.  suggested an EC disinfection system employing a honeycombed platinum-coated titanium electrode for the disinfection of seawater. Cell suspensions of the fish pathogens, Vibrio alginolyticus, Edwardsiella tarda, Lactococcus garvieae and Vibrio anguillarum were circulated in a reactor provided with 10 sets of these electrodes at a flow rate of 200 mL/min with an applied potential of 1.0 V vs. Ag/AgCl reference electrode. The circulated cells were totally killed after 3 h of treatment, whereas free residual Cl2 generated due to seawater electrolysis was below 0.1 mg/L. Moreover, a diphenyl-1-pyrenylphosphine fluorescent assay showed that lipid peroxidation in the cell membranes of disinfected bacteria was induced probably by ROSs produced in the course of EC application.
Hashim et al.  suggested a novel combined ultrasonic-electrocoagulation device (U-ECG setup) to kill E. coli in water. The U-ECG reactor is composed of an ultrasonic bath fitted with four perforated Al electrodes, which are designed to serve as baffle-plates to improve the water-mixing phenomenon. The novel U-ECG device neutralized 100% of the E. coli during 11 min of application instead of 23 min for ECG.
Cotillas et al.  worked on merging iron ECG (Fe-ECG) and UV irradiation (photo-ECG) for eliminating turbidity and E. coli from real treated municipal wastewaters. Sole Fe-ECG was found very performant even at low CDs. E. coli is retained not only via the enmeshment of mechanism into flocs  , but also via the attack of electrochemically formed chlorine disinfectant species. Integrating UV irradiation with Fe-ECG ameliorates the technology effectiveness in dealing with E. coli and turbidity. There is a synergistic interaction of both methods at low CD (1.44 A/m2) but an antagonistic impact at higher levels of CD (7.20 A/m2). Such an antagonistic impact is provoked by the less efficacious transmission of UV irradiation to the bulk solution due to the elevation in the level of colloids.
Rodríguez-Chueca et al.  implemented the Fenton-like techniques induced via radiofrequency for neutralizing fecal bacteria (E. coli and Enterococcus sp.) existing in treated domestic wastewater effluents. Fenton techniques were performed at pH 5 with various iron sources, like iron salts (ferric chloride, 5, 50 and 100 mg/L Fe3+), magnetite (1 g/L) and clay (80 g/L), H2O2 (25 mg/L) and in absence and presence of radiofrequency. Two distinct electromagnetic field intensities (1.57 and 3.68 kA/m) were employed in the Fenton techniques induced by radiofrequency. Ferromagnetic material/H2O2/radiofrequency techniques attained interesting findings in killing bacterial cells. For example, Fe3+/H2O2/radiofrequency attained a maximum degree of E. coli demobilization of 3.55 log following 10 min of application. Such performances are bigger than those recorded in the absence of radiofrequency are. Activating thermally iron atoms lets the Fenton reaction to intensifying, improving the final efficiency of the technique. In addition, distinct behavior was noted in killing E. coli and Enterococcus sp. due to the structural differences between Gram-negative and Gram-positive bacteria  .
Heffron et al.  suggested the removal of viruses by utilizing ECG as a pretreatment prior to EO treatment using BDD electrodes. They employed bench-scale and batch setups to assess the alleviation of viruses via EO and a sequential ECG-EO treatment train. They found that EO of two bacteriophages (MS2 and FX174) was restrained by NOM and turbidity, showing the possible demand for pretreatment. Nonetheless, the ECG-EO treatment train was useful only in the model surface waters tested. In model groundwater, ECG single was as performant as the merged ECG-EO treatment train. Neutralizing human echovirus was considerably smaller than one or both bacteriophages in all model waters; nevertheless, bacteriophage FX174 was a more representative surrogate than MS2 in the occurrence of NOM and turbidity. Juxtaposed to traditional treatment by ferric salt coagulant and free chlorine disinfection, the ECG-EO reactor was less efficient in model surface waters but more performant in model groundwater. Successive ECG-EO was helpful for many implementations, even if engineering factors could presently outbalance the merits.
Bruguera-Casamada et al.  worked on the disinfection of raw dairy wastewater by using a successive treatment involving an ECG stage with a Fe-Fe reactor pursued by electro-Fenton or ultraviolet (UV) A (315 nm - 400 nm)   (UVA)-assisted photo-electro-Fenton. The two latter techniques were performed with an air-diffusion cathode for H2O2 formation and either a BDD or a RuO2-based anode. They examined the demobilization of heterotrophic and lactic acid bacteria, E. coli and enterococci. A modest reduction of the organic load was observed in all circumstances, while the microbes were deficiently retained by the flocs produced in ECG but considerably demobilized in electro-Fenton and photo-electro-Fenton. Compared to ECG, electro-Fenton was of value as it avoided the generation of toxic sludge carrying active bacteria. In the consecutive ECG/electro-Fenton method implying a BDD anode in the latter stage, the killing yield for the lactic acid bacteria was more important at neutral pH, thanks to the large capacity of formed Cl2 to oxidize the molecules of the cell walls. Moreover, employing a RuO2-based anode conducted to a rapid neutralization at pH 3.0. A better achievement was recorded if photo-electro-Fenton substituted electro-Fenton, regardless of the anode, thanks to the improved bacterial demobilization by UVA radiation.
Anodic ECG techniques could eliminate large sets of contaminants in industrial wastewater even if some stubborn pollutants can stay in effluents following the treatment and provoke environmental problems. To elevate the performance of eliminating contaminants, Fan et al.  combined electrocatalysis with ECG and implemented an atomic layer deposition (ALD) that enabled TiO2 ultrathin overcoating at a nanometer scale on a stainless steel cathode. The electrocatalytic overcoating augmented the reduction performance of organic compounds and microbes, mainly thanks to the electro-formation of appropriate ROSs. By employing the new ECG-electrocatalysis reactor to deal with synthetic wastewater, interesting reductions of 99.92% of E. coli, 92.1% of suspended solids, 98.3% of heavy metal ions, and 88.8% of methylene blue were noted. Such an integrated EC technology could lead to treating wastewater at an industrial scale.
8. Disinfection By-Products (DBPs) Formation: An Electrochemical (EC) Disinfection Undesirable Side Effect
As mentioned in the previous Section, chemical water treatment issues such as DBPs formation have incited on the search of better water treatment means such as EC water processes that have been tested with large success in various water/wastewater pollutant treatments . However, their large use is blocked by many technical issues such as DBPs especially chlorine by-products (CBPs) produced species  . In fact, in the course of EC treatment, these carcinogenic products may be generated following the electrode material and applied voltage. In our previous review paper , we have discussed the dependence of CBPs produced species generation of the electrode material and applied charge in the course of EC treatment. It was deduced that the usage of electrodes generating highly reactive species has to be more cautiously monitored in hygienically and environmentally oriented using. Following this orientation, Pt and BDD anodes are proved more appropriate than other electrodes. In fact, the good capacity of a BDD anode to generate ROSs and other oxidizing species during the electrolysis allows establishing a chlorine-free disinfection process .
ECG could be incorporated ahead of microfiltration (MF) to efficiently remove turbidity, microbes, and DBPs and together keep an elevated MF specific flux . Indeed, ECG efficaciously eliminates hydrophobic natural organic matter (NOM) and pathogens. As seen above, ECG effectively removes viruses via physically encapsulating them in flocs, neutralizing their surface charge and decreasing electrostatic repulsion, and enhancing hydrophobic interactions between any sorbed NOM and free viruses . Chellam and Sari  concluded that ECG attains DBP control via reducing NOM, decreasing chlorine-reactivity of the residual NOM.
Bergmann and Koparal  concluded that practical setups must be conceived and monitored in a sophisticated manner. The actual state of non-monitored use of disinfection devices is not favorable in terms of hygienic and health risks considerations. Great works remain to be performed.
Employing mixed metal oxide anodes has been proved for disinfecting water with reduced formation of CBPs. However, more attention is required to improve the technology . Table 3 lists the dares encountered in the water treatment industry related to EC disinfection .
Xu et al.  studied the ECG of landfill leachate during which the formation of chlorine species could lead to the production of toxic DBPs. They investigated such a generation via observing five categories of DBPs (haloacetic acids-HAAs, THMs, haloacetonitriles-HANs, haloketones-HKs, and halonitromethanes-HNMs) in two leachate samples treated by ECG. It was illustrated that the applied current has induced the production of DBPs that were prevailed by unregulated DBPs. With a CD of 100 mA/cm2, the unregulated HKs prevailed the weight-based DBP level (96% in Leachate A and 44.3% in Leachate B), while the unregulated HANs took part in >80% of the DBPs additive toxicity in both leachates. The in
Table 3. Dares in the water treatment industry related to EC disinfection .
situ formations of active chlorine has conducted to the DBP production, as illustrated in the scavenging test. Using granular activated carbon as a post-treatment stage can successfully decrease the total DBP level from 295.33 to 82.04 μg/L in Leachate A, conducting to a global DBP reduction of 72.2% and a toxicity decrease of 50%. Considering the controlling level and shortage of toxicity data, the unregulated DBPs have to retain more interest   .
The main important points drawn from this review may be drawn as:
1) Some mechanisms have been suggested to interpret the deadliness of EC application . Such pathways comprise 1) oxidative stress and cell loss of life because of electrochemically produced oxidants, 2) irreversible permeabilization of cell membranes by the placed EF, 3) EO of vital cellular constituents during exposure to electric current or induced EFs, and 4) electrosorption of negatively charged E. coli cells to the anode surface followed by direct electron transfer reaction   . Physical elimination via enmeshment in ECG flocs is the main mechanism of bacteria reduction in the occurrence of HCO− 3, which greatly reduces demobilization, probably due to a decrease in the lifetime of reactive oxidants . Adhesion of ECG flocs to cell walls, which conducts to microbes’ encapsulation in flocs, is mainly directed by interactions among ECG flocs and phosphate functional groups on bacteria surfaces. ECG flocs’ fixation is a function of the cell wall composition, consistent with comparable densities of phosphate functional groups on Gram-positive and Gram-negative cells   .
2) EFs are by their nature poisonous to microbial cells. Future investigations have to be more dedicated to the EF influence in the EC disinfection, as it is the main part of the involved mechanisms.
3) Employing granular activated carbon post-treatment could greatly reduce the concentrations and poisonous effects of DBPs. Moreover, secure multi-barrier techniques, like distillation (solar disinfection)  , plasma discharge , nanotechnologies , and membrane processes   remain to be suggested, tested, and industrially encouraged. Despite their limitations, both adsorptive techniques and membrane processes persist to be an encouraging domain of research thanks to their relatively low costs and ease of applications   .
The Research Deanship of University of Ha’il, Saudi Arabia, through the Project RG-191190, has funded this research.
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