Electrochemical pretreatment and anaerobic digestion (AD), as well as a combination of both processes, were studied for the treatment of waste-activated sludge (WAS) to evaluate microbial inactivation, for faecal coliforms, Salmonella spp., bacteriophages, and helminth eggs. Electrooxidation (EO) of WAS was performed in a commercial cell with boron-doped diamond electrodes. 1 L of WAS (3% total solids) was fed to the electrochemical cell in recirculation mode. The conditions tested were 19.3 mA/cm2, 30 min, and 3.8 L/min. For AD tests, raw and pretreated WAS were digested in an OxiTop® OC 110 apparatus for 15 days. Inactivation of faecal coliforms, Salmonella spp., and bacteriophages reached more than 5 logs when EO was combined with AD. In contrast, EO alone did not inactivate these parameters, while AD achieved eliminations around 3 logs. Moreover, the combined process inactivated 91% of the initial viable helminth eggs, considerably higher than AD (29%) and EO (0%). The results suggest that EO separates extracellular polymeric substances and segregates particles, including microorganisms, that are exposed to environmental factors (e.g., volatile fatty acids or ammonia) during AD, showing a synergistic effect.

  • Electrooxidation (EO) was not able to inactivate pathogens in sludge.

  • The combination of EO and anaerobic digestion (AD) promotes a synergistic effect on microbial inactivation, including helminth eggs.

  • Separation of extracellular polymeric substances and segregation of sludge particles during EO expose microorganisms to environmental factors in AD, causing their inactivation.

Sewage sludge is the main by-product generated during wastewater treatment and its management is always a concern. After treatment, biosolids (stabilized sludge) can be reused as fertilizer or soil amendment depending on their organic matter and nutrient content, and this pathway allows recycling of large quantities of sludge generated each year, which in most cases increases crop yields and has proven to be beneficial for soils. In addition, a transition toward a circular economy has been proposed in which sludge is used as a source of various by-products such as construction materials, adsorbents, and fertilizers, among others (Collivignarelli et al. 2019). This alternative becomes relevant, prompting the evaluation since it is estimated that the annual sludge production in the world is of the order of 45 Mt (Gao et al. 2020).

Traditionally, sludge stabilization processes have been aerobic digestion, anaerobic digestion (AD), composting, and lime stabilisation. In this particular case, AD is commonly used because it is a sustainable technology that produces a stable humus-like product, reduces the mass of solids to be managed, generates energy in the form of biogas, and the product usually meets regulations (Piadeh et al. 2023).

AD is commonly applied to a mixture of primary and secondary sludge; however, primary sludge is easily biodegradable in contrast with secondary sludge that is formed by biomass and extracellular polymeric substances (EPS) that may be difficult to degrade (More et al. 2014). Moreover, EPS constitutes between 60 and 80% of secondary sludge generated in activated sludge processes (waste-activated sludge, WAS), and they are tightly bonded to microorganisms, which protects them from being lysed and reduces the conversion of organic matter in the process (Li et al. 2021; Yuan et al. 2021).

WAS pretreatment has been applied to improve biogas production during AD. This pretreatment includes a variety of processes that focus on the hydrolysis of microbial cells and EPS to increase soluble organic matter (Carrère et al. 2010; Kim et al. 2013; Yang et al. 2023). More recently, electrooxidation (EO) has been applied as a sludge pretreatment for AD with positive results, including higher and faster methane production (Yu et al. 2014; Yuan et al. 2016; Barrios et al. 2017, 2021).

Electrochemical processes are getting attention due to their capacity to produce highly oxidizing radicals (Zhang et al. 2024). In particular, the use of boron-doped diamond (BDD) electrodes has been widely reported as one of the most stable materials for electrochemical applications (Souza et al. 2016). However, the use of EO for sludge disinfection has seldom been reported, and the few studies that have been applied under controlled conditions (modified pH, helminth eggs spiking) have only measured bacteria, or have employed electrode materials different than BDD (Drogui et al. 2013; Reza Rahmani et al. 2015; Jafari & Botte 2021). Although mesophilic AD can reduce bacterial and viral pathogens, helminth eggs need temperatures above 60 °C to be significantly inactivated (Maya et al. 2012). The literature on the inactivation of helminth eggs in AD, on the other hand, indicates that they are not significantly reduced under mesophilic conditions (32–38 °C) and further studies are needed and may not be applicable in developing countries where sludge contains large amounts of these structures (US EPA 2023; Patil & Mutnuri 2024).

In particular, helminths represent a public health problem in many countries, and an estimated 2.5 billion people are infected by these parasites (Jiménez et al. 2016). Their detection and inactivation are some of the most difficult tasks in wastewater and sludge treatment, with Ascaris eggs being the most widespread genus and considered endemic in Latin America, Africa, and the Far East. Furthermore, Ascaris eggs are the most resistant microorganisms in sludge, which is attributed to the highly resistant eggshell and the chemical arrangement of its membrane (Jiménez 2007; Mahapatra et al. 2022).

Over the last decade, research has explored the coupling of different treatment processes that have proven to be effective for wastewater or sludge disinfection by (a) increasing disinfection efficiency; (b) broadening the spectrum of microorganisms that can be inactivated; (c) reducing the number of reagents used and thus the risk of environmental toxicity; and (d) reducing operating costs (Maya et al. 2012; Cano et al. 2016; Cotillas et al. 2016; Zeng et al. 2019). However, most reports dealt with sewage sludge with TS and volatile solids (VS) content in the range of 5.18–21.8 and 4.23–14.4 g/L, respectively, (Zeng et al. 2019; Arenas et al.. 2021; Xi et al. 2022). For this reason, this work reports the synergistic effect of EO and AD of sewage sludge to inactivate microbial indicators, including helminth eggs, which are particularly resistant to conventional treatment processes.

Collection and preparation of WAS samples

WAS was collected from a municipal wastewater treatment plant located in Mexico City, Mexico. Samples obtained from the wasting pipe of the secondary settling tank were transported in 50 L plastic containers to the laboratory and stored at 3 °C until their use. Sludge total solids were adjusted to 3% by sedimentation (2 h) and supernatant decantation, followed by centrifugation at 1,400 g for 20 min (Beckman Coulter, Avanti J-26S XPI centrifuge) and adjusted accordingly.

Electrochemical process

WAS EO was performed in a commercial electrochemical cell (DiaClean®, WaterDiam Sarl, Switzerland) with BDD electrodes with 70 cm2 of active surface. 1 L of sludge (3% total solids, TS) was fed to the electrochemical cell from a mixed temperature-controlled vessel (25 °C) with a peristaltic pump (Cole-Parmer, model 7553-20) in recirculation mode. The conditions tested were 19.3 mA/cm2, 30 min, and 3.8 L/min, which were reported as the best operating conditions for pretreating WAS to maximize methane production by Pérez-Rodríguez et al. (2019). Before EO tests, samples were sieved through a 1.0 mm mesh to avoid cell clogging. After each test, the electrochemical cell was cleaned for 30 min with a sodium sulfate solution (0.5% m/v) adjusted to a pH of 2 with sulfuric acid and applying a current density of 19.3 mA/cm2 and a flow of 3.8 L/min based on Pereira et al. (2012).

AD treatment

To perform the AD tests, raw and pretreated WAS were digested in an OxiTop® OC 110 apparatus (WTW, Germany), which consists of 12 serological bottles of 250 mL with a working volume of 80 mL where biogas production was automatically measured at 160-min intervals. The operating conditions were: food to microorganism (F/M) ratio of 0.15 g SVfed/g SVbiomass, 38 °C of temperature, pH adjusted to 7, and shaking at 150 rpm for 15 days as reported by Barrios et al. (2017).

Chemical analysis

Total and volatile solids as well as total and soluble chemical oxygen demand (COD) were determined following the Standard Methods (APHA-AWWA-WEF 2017), before and after electrochemical pretreatment and AD. Soluble COD was performed by centrifuging a WAS sample (1,400 g for 15 min) and then filtering the supernatant through a 0.45 μm filter. Conductivity, pH, and temperature were measured with Thermo Scientific model Orion Star A329 equipment.

Microbiological analysis

Representative organisms commonly found in sludge were selected for triplicate analyses: (a) viruses (somatic bacteriophages), (b) bacteria (faecal coliforms and Salmonella typhi), and (c) helminth eggs. Analytical techniques used for these microorganisms were the following:

  • i. Bacteriophages: dual layer method ISO 10705 with Escherichia coli strain CB390 WG5 after Grabow & Coubrough (1986).

  • ii. Bacteria (APHA AWWA WEF 2017).

    • a. Faecal coliforms: direct technique with Medium A-1 (Method 9221-E)

    • b. S. typhi: in the pre-enrichment and enrichment broths (Method 9260-B).

  • iii. Helminth eggs: sludge samples were liquefied by stirring with 1 L of Tween 1% and filtered through the combination of 150 and 20 μm sieves, the sample recovered was transferred into a 200 mL centrifuge container and centrifuged at 660 g for 10 min. Subsequently, the supernatant was discarded and the pellet was suspended with a solution of zinc sulfate (ZnSO4; density: 1.3). The Sample was then centrifuged at 660 g for 10 min and the supernatant was filtered by a 20 μm sieve, and rinsed with tap water. The recovered sample was subsequently centrifuged and the final pellet was transferred to a Sedgewick-Rafter counting chamber, to identify and quantify helminth eggs by direct observation at the optic microscope (Maya et al. 2012).

Physicochemical and microbiological characterization of WAS

Table 1 shows the physicochemical and microbiological characteristics of WAS once total solids were adjusted to 3%. Physicochemical parameters, such as pH, conductivity, volatile solids, and total and soluble COD, were similar to values reported previously (Pérez-Rodríguez et al. 2019). WAS exhibited a neutral pH with close to 70% organic matter (volatile solids), and most of it was associated with particle organic matter as less than 0.4% of the COD is soluble. Concerning microbial parameters, the levels found in WAS agree with other studies (Jiménez et al. 2004; Ruiz-Hernando et al. 2014). It should be recalled that helminth eggs are related to particulate matter; as a result, their concentration is generally higher in primary sludge than in WAS, as the former comes from primary sedimentation where most of the wastewater solids are removed.

Table 1

Physicochemical and microbiological characteristics of untreated WAS at 3% total solids

ParameterValue
pH 6.7 ± 0.1 
Conductivity, μS/cm 1,350 ± 3.54 
Total solids, % 3.01 ± 0.8 
Volatile solids, % of TS 68.97 ± 1.66 
Chemical oxygen demand (total COD), mg O2/L 34,612 ± 1,733 
Chemical oxygen demand (soluble COD), mg O2/L 123 ± 15 
Faecal coliforms, log10 MPN/g TS 7.66 ± 0.34 
Salmonella spp., log10 MPN/g TS 5.47 ± 0.11 
Bacteriophages, log10 PFU/g TS 7.04 ± 0.26 
Helminth eggs, total eggs/g TS 12.67 ± 1.44 
ParameterValue
pH 6.7 ± 0.1 
Conductivity, μS/cm 1,350 ± 3.54 
Total solids, % 3.01 ± 0.8 
Volatile solids, % of TS 68.97 ± 1.66 
Chemical oxygen demand (total COD), mg O2/L 34,612 ± 1,733 
Chemical oxygen demand (soluble COD), mg O2/L 123 ± 15 
Faecal coliforms, log10 MPN/g TS 7.66 ± 0.34 
Salmonella spp., log10 MPN/g TS 5.47 ± 0.11 
Bacteriophages, log10 PFU/g TS 7.04 ± 0.26 
Helminth eggs, total eggs/g TS 12.67 ± 1.44 

MPN: most probable number; PFU: plaque-forming units

EO pretreatment

WAS EO showed an effect in the particulate organic matter as soluble COD showed an increase from 123 to 625 mg/L. This solubilization is caused by the lysis of microbial cells after they are attacked by hydroxyl radicals generated at the surface of the electrode. To evaluate this change, the degree of solubilization was determined according to Appels et al. (2010), resulting in 1.45% solubilization consistent with previous reports (Pérez-Rodríguez et al. 2019). Even though this seems like a small value, AD after an EO pretreatment under similar conditions has resulted in higher biogas yields (up to 80% more) compared to untreated WAS (Barrios et al. 2017).

After EO of WAS, microbial indicators did not show a considerable reduction (<0.2-log10 and 0% for helminth eggs; Table 2), which is attributable to the difficulty of the microorganisms to come into contact with the active electrode surface where hydroxyl radical generation takes place. After WAS EO, microbial indicators did not show a considerable reduction (<0.2-log10 and 0% for helminth eggs; Table 2), which is attributable to the difficulty of the microorganisms to come into contact with the active electrode surface where hydroxyl radical generation takes place. It is important to mention that the operating conditions were taken from previous studies to maximise methane production in AD and are not necessarily optimised for microbial inactivation (Pérez-Rodríguez et al. 2019). It should be recalled that hydroxyl radicals are not capable of migrating to the solution (in this case, bulk WAS) as they are short-lived (10−9 s; Louit et al. 2005). Nonetheless, Jeong et al. (2006) reported that electro-generated hydroxyl radicals are the main species that cause inactivation of E. coli. Moreover, under the operating conditions studied (current density and treatment time) as well as the high amount of organic matter present in sludge, the generation of secondary oxidants (such as sodium hypochlorite) is presumed to be negligible. In addition, microorganisms, as well as helminth eggs, are associated with solid particles that protect them from disinfection processes (Brahmi et al. 2010), and EPS also protects them. Ruiz-Hernando et al. (2014) suggested that ultrasonication of WAS dissipated the flocs but was not able to inactivate bacteria or bacteriophages. In the case of helminth eggs, their lipidic membrane adheres to solid particles, such as biomass and flocs, which protects them from the attack of hydroxyl radicals inside the electrochemical cell.

Table 2

Inactivation of selected microbial indicators

TreatmentFaecal coliformsaSalmonella spp.aBacteriophagesaHelminth eggs, %
EO 0.05 0.00 0.15 
AD 3.06 3.42 3.17 29 
EO + AD 5.52 5.30 5.60 91 
TreatmentFaecal coliformsaSalmonella spp.aBacteriophagesaHelminth eggs, %
EO 0.05 0.00 0.15 
AD 3.06 3.42 3.17 29 
EO + AD 5.52 5.30 5.60 91 

alog10 units.

Note. EO, electrooxidation; AD, anaerobic digestion; EO + AD, electrooxidation followed by anaerobic digestion.

Faecal coliform inactivation for EO is similar to that reported by Hu et al. (2021a), where marginal reductions were observed (<1 log10). The same authors reported that when EO was combined with the addition of iron [Fe(II)], the process caused a significant reduction of pH and increased temperature in the sludge, but still reduced by less than 2 log10 units. Moreover, studies using EO alone or combined with hypochlorous acid addition agree on a small inactivation of faecal coliforms (<0.3 log10 units) when EO was evaluated and suggest that chemical addition is more relevant for bacteria reduction (Hu et al. 2021b).

Other authors similarly report that the application of electrofenton for disinfecting spiked synthetic water was not able to significantly reduce microbiological indicators, including helminth eggs (Robles et al. 2020). It is important to mention that helminth eggs have a membrane composed of several layers of lipids, chitin, and proteins, which together act as a protective barrier to adverse environmental conditions and make them resistant to common disinfection processes, but certain organic acids, such as acetic and peracetic, as well as ammonia, may inactivate them (Mendez et al. 2002; Jiménez 2007). Even though the EO of certain organic compounds may result in the production of carboxylic acids (Barrios et al. 2015; Oliveira et al. 2023), including acetic acid, their concentration in this study is assumed to be negligible for disinfection purposes as pH exhibited a slight increase (final pH: 6.9–7.1). It should be noted that VFA concentration reached up to 1.17 g HAc/L in pretreated sludge, which appears insufficient to inactivate the microbial parameters tested.

Anaerobic digestion

AD alone showed a considerably higher inactivation than EO. Faecal coliforms, Salmonella spp., and bacteriophages were reduced by 3.06, 3.42, and 3.17 log10, respectively (Figure 1); however, helminth eggs were only partially inactivated (29%; Figure 2). It should be recalled that helminth eggs are highly resistant structures that are not always inactivated through conventional treatment processes. Manser et al. (2015a) obtained a similar inactivation of Ascaris suum eggs (∼30%) when sludge was anaerobically digested for 15 days. In contrast, these results differ from those reported by Forster-Carneiro et al. (2010), where mesophilic AD eliminated pathogens such as Salmonella spp., but agree on the fact that helminth eggs are not fully inactivated. Also, bacteria reductions are consistent with those of Manser et al. (2015b), who reported the survival of Salmonella and E. coli (no more than 3-log10 removal). Moreover, the results are within the range stated for AD, except for bacteriophages, which reported a reduction between 0.5 and 2.0 logs (US EPA 2023). It should be noted that microbial inactivation during AD is attributed to several factors, including temperature, solids retention time, volatile fatty acids (VFA), and ammonia concentration, as well as competition among species; however, the responsible mechanisms are still not fully understood (Zhao & Liu 2019). In this respect, previous studies with raw WAS reported a VFA concentration of 3.36 g HAc/L (Barrios et al. 2017), a relatively high value for conventional digestion, but did not achieve complete microbial inactivation, which may be attributed to the fact that the sludge was not pretreated and unhydrolyzed EPS may protect microorganisms.
Figure 1

Faecal coliforms, Salmonella spp., and bacteriophages in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment).

Figure 1

Faecal coliforms, Salmonella spp., and bacteriophages in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment).

Close modal
Figure 2

Helminth eggs in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment; V: viable eggs; NV: non-viable eggs).

Figure 2

Helminth eggs in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment; V: viable eggs; NV: non-viable eggs).

Close modal

Synergism between EO and AD

The combination of EO and AD demonstrated the synergism between these technologies. Faecal coliforms and bacteriophages were reduced by 5.52 and 5.60 log10 units (Table 2). Even though they were not completely inactivated, their final concentrations easily meet those established in most regulations. Some authors suggest that the adsorption of viruses and bacteriophages to solid particles reduces their exposed surface and protects them from different substances (Martín-Díaz et al. 2020). On the other hand, the process achieved complete inactivation of Salmonella spp., which may be explained by the fact that these bacteria are partially sensitive to temperature but highly sensitive to VFAs, such as those produced during AD (Zhao & Liu 2019). It should be noted that previous EO tests under similar conditions reached a VFA concentration of 2.69 g HAc/L after sludge hydrolysis (Barrios et al. 2017), although in this case, this value should be lower according to soluble COD. Nonetheless, as sludge flocs are broken during pretreatment, microorganisms may be fully exposed to such acids. Further analyses (Figure 3) indicate that the inactivation of faecal coliforms, Salmonella spp., and bacteriophages follows a similar trend, with the highest removal obtained with the combined treatment (EO + AD). These results agree with García-Aljaro et al. (2019) who state that ‘indicator bacteria are still the preferred choice to assess water quality and water treatments operation’ as demonstrated by pathogenic Salmonella spp. behaving similarly after sludge treatment.
Figure 3

Relative inactivation of faecal coliforms, Salmonella spp., and bacteriophages in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment).

Figure 3

Relative inactivation of faecal coliforms, Salmonella spp., and bacteriophages in raw (WAS) and treated sludge (EO: electrooxidation; AD: anaerobic digestion; EO + AD: combined treatment).

Close modal

Finally, helminth eggs were inactivated by 91%, which allows the sludge to comply with most Class B regulations (considering viable eggs). As mentioned before, these eggs are highly resistant structures, but their membrane is permeable to organic acids and ammonia. Since EO modifies the sludge structure by breaking the flocs and the EPS that protect solid particles, it appears that bacteria and helminth eggs become separated from those particles, exposing them to potentially toxic compounds (such as VFAs or ammonia) and, in the case of bacteria, also to competing organisms, which would cause their inactivation. As a reference, prior studies have demonstrated a particle size reduction of more than 42% after sludge EO with BDD electrodes, which supports this theory (Cazares et al. 2021). Based on these results, it is clear that eggs are segregated and then inactivated, rather than destroyed, as they were still present after viability tests, but they did not develop larvae.

In this study, EO did not reduce microbial indicators while AD demonstrated a partial reduction of bacteria and bacteriophages (3.06–3.42 log10 units). In addition, none of those processes achieved the inactivation of helminth eggs. However, the combination of EO and AD reduced bacteria and bacteriophages by more than 5 log10 units and more than 90% of viable helminth eggs. These combined processes have already proven effective for increasing organic matter degradation and biogas production and now demonstrate their applicability to reduce the microbial content and comply with different regulations.

In addition, these results demonstrate the synergistic effect of EO followed by AD in the inactivation of bacteria, bacteriophages, and helminth eggs in sludge. Based on prior studies and the literature, EO separates EPSs and segregates particles, including microorganisms and helminth eggs, that become exposed to environmental factors (e.g., VFA or ammonia) during AD. This exposition causes the inactivation of helminth eggs rather than destruction as they were still present after the combined treatment, but additional tests showed they were not viable. Future studies should focus on optimising the operating conditions (i.e., current density, flow, and treatment time) for microbial inactivation in AD.

Funding was provided by Instituto de Ingeniería UNAM (Proy. R255)

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.

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Supplementary data