Abstract

The fate of pathogen indicators (Escherichia coli – EC, intestinal enterococci – IE, RNA-F bacteriophages and spores of sulfite reducing bacteria – SSR) was extensively studied in Parisian large-scale wastewater treatment plants (WWTPs), based on conventional activated sludge, biofiltration or membrane bioreactor (MBR) processes. Between 14 and 87 campaigns were performed between 2014 and 2018 in five WWTPs. High removals of 3 log for both EC and IE, and lower removals of 1–2 log for SSR and RNA-F bacteriophages, were observed in conventional activated sludge and biofiltration WWTPs. The MBR WWTP achieves notably greater removals of 4.5–5.5 log for faecal bacteria and 3–4 log for SSR and RNA-F bacteriophages. This WWTP is the only one already in compliance with reuse standards, the other ones being non-compliant because of SSR and RNA-F bacteriophages. The implementation of a micro-grain activated carbon process would increase the WWTP removals of 0.8 log for faecal bacteria, due to particles retention, with no significant effect on both other pathogens. Ozonation (0.9–1.3 g O3/g dissolved organic carbon) or performic acid (0.8–1.2 ppm) would have greater benefits with additional removals of 1.5–2.5 log for EC, 1–2 log for IE and 0.5–1 log for SSR and RNA-F bacteriophages. Correlations between pathogen indicator removals and initial concentrations were found, as well as a significant decrease of RNA-F bacteriophage concentrations in Parisian raw wastewater, below 2 log. Thus, RNA-F bacteriophages could be a real issue to evaluate the compliance of Parisian wastewater with reuse. The time evolution of removals demonstrated that SSR is the most problematic parameter regarding reuse in conventional activated sludge and biofiltration WWTPs, as its initial concentration is high (5 log) but removals insufficient (<2 log). In contrast, removals of RNA-F bacteriophages greater than 2 log can be obtained within WWTPs completed or not with a tertiary treatment when the initial concentration in raw wastewater is sufficient. Correlations were also found between the removals of pathogen indicators and the removals of physico-chemical parameters, but they are not good enough to allow performance predictions.

HIGHLIGHTS

  • The fate of pathogen indicators was studied in five large WWTPs.

  • Biofiltration removes 2.7–3.4 log of faecal bacteria, 0.9–1.2 log of RNA-F bacteriophages and 1.5–1.7 log of SSR.

  • Pathogen indicator removals are 1–3 log higher in MBR compared to conventional biological processes.

  • μGAC treatment can refine faecal bacteria concentrations while ozone or PFA also partly remove RNA-F bacteriophages and SSR (0.5–1.0 log).

INTRODUCTION

Wastewater treatment plants (WWTPs) are currently designed to efficiently remove physico-chemical parameters to cope with European standards (Directive 91/271/EEC 1991; Directive 2000/60/EC 2000). Thus, pathogen indicators are not targeted or monitored by wastewater operators. However, the evolution of societal expectations in urban areas and the context of climate change, which will result in increasing water scarcity, are in favor of an expansion of wastewater reuse. Currently, wastewater reuse is regulated by the Arrêté du 25 juin 2014 in France. It fixes quality categories, with associated authorized uses, which are based on total suspended solids (TSS), chemical oxygen demand (COD) and Escherichia coli (EC) and on intestinal enterococci (IE) concentrations, removals of RNA-F bacteriophages and spores of sulfite reducing bacteria (SSR). Data about the fate of pathogen indicators in full-scale WWTPs based on the three most employed processes, conventional activated sludge, biofiltration and membrane bioreactor (MBR), are scarce in the literature with only nine papers found by the authors (Ottoson et al. 2006; Zhang & Farahbakhsh 2007; Wen et al. 2009; Fu et al. 2010; Zanetti et al. 2010; De Luca et al. 2013; Montazeri et al. 2015; Purnell et al. 2016; Dias et al. 2018). In particular, only one paper was found for biofiltration (Dias et al. 2018) but it deals with a small-scale WWTP. MBR at full-scale is also poorly documented with four papers (Ottoson et al. 2006; Zanetti et al. 2010; De Luca et al. 2013; Purnell et al. 2016), only one for a large-scale WWTP (Purnell et al. 2016). In addition, they do not study the four pathogen indicators, few data were found for RNA-F bacteriophages and no data for SSR. This paper presents the results from an extensive monitoring of the four pathogen indicators within five large-scale Parisian WWTPs. Between 14 and 87 campaigns were conducted depending on the parameter and the WWTP between 2014 and 2018. In addition, the data collected on those pathogen indicators during the study of three tertiary treatments (micro-grain activated carbon, ozone, performic acid) applied to the Parisian treated wastewaters were synthetized to evaluate the supplementary removals that can be expected in case of implementation (Mailler et al. 2015, 2016; Guillossou et al. 2019, 2020). The collected data allow display of the achieved removals for EC, IE, RNA-F bacteriophages and SSR in large-scale WWTPs based on activated sludge, biofiltration and MBR, and in the same WWTPs upgraded by tertiary treatments. This large database is also used to evaluate the correlations that can be observed between the removals of pathogen indicators and their concentrations and physico-chemical parameters. Finally, the evolution of those pathogen indicators between 2014 and 2018 in Parisian wastewaters was studied and a temporal evolution was found for RNA-F bacteriophages. All the results are used to discuss their implications regarding wastewater reuse, and the technical choices and lack of precision in the regulation, identified by authors, which can limit the extension of wastewater reuse or force including additional tertiary treatment.

MATERIALS AND METHODS

Description of Parisian WWTPs

Five WWTPs, operated by SIAAP (the Greater Paris Sanitation Authority, in charge of wastewater collection and treatment), were considered in this study. They represent a total capacity of more than 2,600,000 m3/day. Seine Aval (SAV) has a capacity of 1,500,000 m3/day and treats wastewater from the entire Parisian conurbation based on biofiltration. This WWTP was recently (2017) completed by an MBR line treating 10 to 25% of the WWTP flow. Seine Valenton (SEV) has a capacity of 550,000 m3/day and treats wastewater from the eastern part of the Parisian conurbation based on conventional activated sludge. Seine Grésillons (SEG) has a capacity of 300,000 m3/day and treats wastewater from the western part of the Parisian conurbation based on biofiltration. Seine Centre (SEC) has a capacity of 240,000 m3/day and treats wastewater from Paris city based on biofiltration. Seine Morée (SEM) has a capacity of 50,000 m3/day and treats wastewater from the northern part of the Parisian conurbation based on MBR technology. The complete technical description of these WWTPs is given in Supplementary Information – Table S1.

Sampling, analyses and data treatment

The fate of pathogen indicators in Parisian WWTPs was evaluated considering all data available in SIAAP between 2014 and 2018 including EC, IE, RNA-F specific bacteriophages and SSR. These indicators are not monitored on a daily basis in SIAAP facilities as they are not part of regulatory monitoring but the available data represent 42–114 values for EC, 42–114 values for IE, 19–40 values for RNA-F or 27–77 values for SSR depending on the WWTP. They were collected by the SIAAP Innovation Department in both inlet and outlet of the facilities. Samples were 24-h composite samples collected with automated samplers. These indicators were measured according to the following norms: NF EN ISO 9308-3 for EC, NF EN ISO 7899-1 for IE, NF EN ISAO 10705-1 for RNA-F bacteriophages and NF EN 244621-2 for SSR. The corresponding limits of quantification (LQs) are respectively 15 or 38 MPN/100 mL for both faecal bacteria, 1 PFU/50 mL for SSR and 30 CFU/100 mL for RNA-F bacteriophages.

The results were treated and compared to the French wastewater reuse regulation (Arrêté du 25 juin 2014), establishing water quality standards with authorized uses based on these pathogen indicators and TSS and COD. These quality standards are given in Supplementary Information –Table S2. TSS and COD, as well as N-NH4 and P-PO4, were also considered in this study as indicators of the efficiency of the WWTP processes.

Regarding physico-chemical parameters, data considered in this study were collected from the WWTPs' regulatory monitoring for both raw and treated wastewater. These parameters are measured on a daily basis within 24-h composite samples collected with automated samplers. Analyses were realized by the SIAAP central laboratory according to the following norms: NF EN 872 for TSS, NF T-90-101 for COD, NF EN ISO 11732 for N-NH4 and NF EN ISO 15681-2 for P-PO4. Between 2014 and 2018, the available data represent 765–1,554 values for TSS, COD, N-NH4 or P-PO4 depending on the WWTP.

RESULTS AND DISCUSSION

Efficiency of the Parisian WWTPs to remove pathogens

Fate of faecal bacteria in conventional activated sludge, biofiltration and MBR WWTPs

The five Parisian WWTPs studied are very efficient regarding physico-chemical parameters, as displayed in Supplementary Information – Figure S1. Average removals (2014–2018) of 95.8–99.4% for TSS, 89.8–97.9% for COD, 93.5–99.5% for N-NH4 and 65.9–94.9% for P-PO4 are achieved, with the highest removals achieved in SEM for all parameters thanks to the MBR process.

Regarding the fate of faecal bacteria, average logarithmic concentrations in raw wastewater and average logarithmic removals achieved in the five WWTPs are given in Figure 1, with standard deviations as error bars. In addition, they are compared in Table 1 to the data available in the literature for full-scale WWTPs based on conventional activated sludge, biofiltration or MBR. The Supplementary Information – Table S3 – displays the results of the statistical tests performed to compare the five WWTPs' removals for the four pathogen indicators.

Table 1

Fate of pathogens reported in the literature in full-scale WWTPs based on activated sludge, biofiltration and MBR

ReferenceCountryFaecal bacteria
Other pathogen indicators
Raw wastewater log contentWWTP log removalRaw wastewater log contentWWTP log removal
WWTPs based on conventional activated sludge 
This study (Seine Valenton) France
(600,000 m3/d) 
EC = 7.2 ± 0.6
IE = 6.5 ± 0.5 
EC = 3.2 ± 0.8
IE = 2.9 ± 0.7 
RNA-F = 4.0 ± 1.0
SSR = 3.9 ± 0.7 
RNA-F = 2.1 ± 0.8
SSR = 1.2 ± 0.5 
De Luca et al. (2013)  Italy
(36,000 PE) 
EC = 6.0–7.9
IE = 5.5–6.3 
EC = 2.3
IE = 1.4 
SC = 5.0–6.8
RNA-F = 5.2–7.0 
SC = 2.7
RNA-F = 3.1 
Zhang & Farahbakhsh (2007)  China
(64,000 m3/d) 
TC = 7.4
FC = 7.0 
TC = 4.4–5.4
FC = 4.3–5.7 
SC = 5.5
RNA-F = 5.3 
SC = 3.3–5.2
RNA-F = 3.2–5.5 
Fu et al. (2010)  China
(1,000,000 m3/d) 
FC = 4.6 FC = 2.9 SC = 4.7
Cry = 2.4
Gia = 3.2 
SC = 2.3
Cry = 1.6
Gia = 1.9 
Montazeri et al. (2015)  USA
(370,000 m3/d) 
EC = 6.0 ± 0.1
IE = 5.1 ± 0.1
FC = 6.1 ± 0.1 
4.4 for indicator bacteria MSC = 4.2–4.8 MSC = 1.5 
Dias et al. (2018)  United Kingdom (5,000–45,000 PE) IE = 5.8 ± 0.4
FC = 6.6 ± 0.6 
IE = 2.5
FC = 2.5 
SC = 5.9 ± 0.5
RNA-F = 3.3 ± 0.9
BFP = 3.5 ± 0.8 
SC = 2.1
RNA-F = 1.9
BFP = 2.0 
Wen et al. (2009)  Australia
(135,000 m3/d) 
EC = 6.9–7.4
IE = 5.7–6.9
TC = 7.6–8.2 
EC = 2.2 ± 1.0
IE = 2.0 ± 0.7
TC = 2.3 ± 0.8 
Cry = 4.2–4.4
Gia = 3.4–3.9 
Cry = 0.7 ± 0.4
Gia = 1.4 ± 0.3 
Ottoson et al. (2006)  Sweden
(450 PE) 
EC = NA
IE = NA 
EC = 3.2 ± 0.8
IE = 3.2 ± 0.9 
RNA-F = NA
SC = NA
Cry = 0.7 ± 0.5
Gia = 3.1 ± 0.4 
RNA-F = 3.5 ± 0.8
SC = 2.3 ± 0.6
Cry = 1.6 ± 1.3
Gia = 3.5 ± 0.9 
WWTPs based on biofiltration 
This study (Seine Centre) France
(240,000 m3/d) 
EC = 6.9 ± 0.4
IE = 6.0 ± 0.5 
EC = 3.1 ± 0.7
IE = 3.4 ± 0.7 
RNA-F = 3.8 ± 1.4
SSR = 4.7 ± 0.4 
RNA-F = 1.1 ± 0.6
SSR = 1.7 ± 0.5 
This study (Seine Grésillons) France
(300,000 m3/d) 
EC = 7.1 ± 0.3
IE = 6.3 ± 0.3 
EC = 3.0 ± 0.6
IE = 3.1 ± 0.5 
RNA-F = 3.4 ± 1.3
SSR = 4.8 ± 0.3 
RNA-F = 0.9 ± 0.6
SSR = 1.9 ± 0.4 
This study (Seine Aval) France
(1,500,000 m3/d) 
EC = 7.0 ± 0.3
IE = 6.2 ± 0.3 
EC = 2.7 ± 0.7
IE = 2.8 ± 0.8 
RNA-F = 3.2 ± 1.2
SSR = 4.9 ± 0.4 
RNA-F = 1.2 ± 0.7
SSR = 1.5 ± 0.5 
Dias et al. (2018)  United Kingdom (5,000–45,000 PE) IE = 5.8 ± 0.6
FC = 6.7 ± 0.6 
IE = 1.9
FC = 1.7 
SC = 6.1 ± 0.5
RNA-F = 3.2 ± 0.9
BFP = 3.8 ± 0.7 
SC = 0.6
RNA-F = 0.1
BFP = 0.5 
WWTPs based on MBR 
This study (Seine Morée) France
(50,000 m3/d) 
EC = 7.3 ± 0.9
IE = 6.2 ± 0.5 
EC = 5.5 ± 0.9
IE = 4.7 ± 0.4 
RNA-F = 3.6 ± 0.9
SSR = 4.8 ± 1.0 
RNA-F = 3.1 ± 1.1
SSR = 3.7 ± 1.3 
Zanetti et al. (2010)  Italy
(8,000 PE) 
EC = 6.9 ± 0.4
IE = 5.9 ± 0.2
FC = 7.3 ± 0.4
TC = 8.1 ± 0.8
TTC = 7.4 ± 0.4 
EC = 6.8
IE = 5.8
FC = 7.0
TC = 6.0
TTC = 6.7 
SC = 6.2 ± 0.3
RNA-F = 6.0 ± 0.4
BFP = 3.9 ± 1.7 
SC = 4.5
RNA-F = 5.8
BFP = 3.9 
De Luca et al. (2013)  EC = 6.0–7.9
IE = 5.5–6.3 
EC = 6.8
IE = 5.8 
SC = 5.0–6.8
RNA-F = 5.2–7.0 
SC = 4.3
RNA-F = 5.8 
Ottoson et al. (2006)  Sweden
(450 PE) 
EC = NA
IE = NA 
EC = 5.0 ± 0.9
IE = 4.5 ± 1.1 
RNA-F = NA
SC = NA
Cry = 0.7 ± 0.5
Gia = 3.1 ± 0.4 
RNA-F = 3.8 ± 0.9
SC = 3.1 ± 0.7
Cry = >1.4
Gia = >3.9 
Purnell et al. (2016)  United Kingdom (300,000 PE) IE = 6.0–6.5
FC = 6.7–7.2 
IE = 6.2
FC = 7.0 
SC = 5.5–6.5
RNA-F = 3.2–4.6 
SC = 5.6
RNA-F = 3.9 
ReferenceCountryFaecal bacteria
Other pathogen indicators
Raw wastewater log contentWWTP log removalRaw wastewater log contentWWTP log removal
WWTPs based on conventional activated sludge 
This study (Seine Valenton) France
(600,000 m3/d) 
EC = 7.2 ± 0.6
IE = 6.5 ± 0.5 
EC = 3.2 ± 0.8
IE = 2.9 ± 0.7 
RNA-F = 4.0 ± 1.0
SSR = 3.9 ± 0.7 
RNA-F = 2.1 ± 0.8
SSR = 1.2 ± 0.5 
De Luca et al. (2013)  Italy
(36,000 PE) 
EC = 6.0–7.9
IE = 5.5–6.3 
EC = 2.3
IE = 1.4 
SC = 5.0–6.8
RNA-F = 5.2–7.0 
SC = 2.7
RNA-F = 3.1 
Zhang & Farahbakhsh (2007)  China
(64,000 m3/d) 
TC = 7.4
FC = 7.0 
TC = 4.4–5.4
FC = 4.3–5.7 
SC = 5.5
RNA-F = 5.3 
SC = 3.3–5.2
RNA-F = 3.2–5.5 
Fu et al. (2010)  China
(1,000,000 m3/d) 
FC = 4.6 FC = 2.9 SC = 4.7
Cry = 2.4
Gia = 3.2 
SC = 2.3
Cry = 1.6
Gia = 1.9 
Montazeri et al. (2015)  USA
(370,000 m3/d) 
EC = 6.0 ± 0.1
IE = 5.1 ± 0.1
FC = 6.1 ± 0.1 
4.4 for indicator bacteria MSC = 4.2–4.8 MSC = 1.5 
Dias et al. (2018)  United Kingdom (5,000–45,000 PE) IE = 5.8 ± 0.4
FC = 6.6 ± 0.6 
IE = 2.5
FC = 2.5 
SC = 5.9 ± 0.5
RNA-F = 3.3 ± 0.9
BFP = 3.5 ± 0.8 
SC = 2.1
RNA-F = 1.9
BFP = 2.0 
Wen et al. (2009)  Australia
(135,000 m3/d) 
EC = 6.9–7.4
IE = 5.7–6.9
TC = 7.6–8.2 
EC = 2.2 ± 1.0
IE = 2.0 ± 0.7
TC = 2.3 ± 0.8 
Cry = 4.2–4.4
Gia = 3.4–3.9 
Cry = 0.7 ± 0.4
Gia = 1.4 ± 0.3 
Ottoson et al. (2006)  Sweden
(450 PE) 
EC = NA
IE = NA 
EC = 3.2 ± 0.8
IE = 3.2 ± 0.9 
RNA-F = NA
SC = NA
Cry = 0.7 ± 0.5
Gia = 3.1 ± 0.4 
RNA-F = 3.5 ± 0.8
SC = 2.3 ± 0.6
Cry = 1.6 ± 1.3
Gia = 3.5 ± 0.9 
WWTPs based on biofiltration 
This study (Seine Centre) France
(240,000 m3/d) 
EC = 6.9 ± 0.4
IE = 6.0 ± 0.5 
EC = 3.1 ± 0.7
IE = 3.4 ± 0.7 
RNA-F = 3.8 ± 1.4
SSR = 4.7 ± 0.4 
RNA-F = 1.1 ± 0.6
SSR = 1.7 ± 0.5 
This study (Seine Grésillons) France
(300,000 m3/d) 
EC = 7.1 ± 0.3
IE = 6.3 ± 0.3 
EC = 3.0 ± 0.6
IE = 3.1 ± 0.5 
RNA-F = 3.4 ± 1.3
SSR = 4.8 ± 0.3 
RNA-F = 0.9 ± 0.6
SSR = 1.9 ± 0.4 
This study (Seine Aval) France
(1,500,000 m3/d) 
EC = 7.0 ± 0.3
IE = 6.2 ± 0.3 
EC = 2.7 ± 0.7
IE = 2.8 ± 0.8 
RNA-F = 3.2 ± 1.2
SSR = 4.9 ± 0.4 
RNA-F = 1.2 ± 0.7
SSR = 1.5 ± 0.5 
Dias et al. (2018)  United Kingdom (5,000–45,000 PE) IE = 5.8 ± 0.6
FC = 6.7 ± 0.6 
IE = 1.9
FC = 1.7 
SC = 6.1 ± 0.5
RNA-F = 3.2 ± 0.9
BFP = 3.8 ± 0.7 
SC = 0.6
RNA-F = 0.1
BFP = 0.5 
WWTPs based on MBR 
This study (Seine Morée) France
(50,000 m3/d) 
EC = 7.3 ± 0.9
IE = 6.2 ± 0.5 
EC = 5.5 ± 0.9
IE = 4.7 ± 0.4 
RNA-F = 3.6 ± 0.9
SSR = 4.8 ± 1.0 
RNA-F = 3.1 ± 1.1
SSR = 3.7 ± 1.3 
Zanetti et al. (2010)  Italy
(8,000 PE) 
EC = 6.9 ± 0.4
IE = 5.9 ± 0.2
FC = 7.3 ± 0.4
TC = 8.1 ± 0.8
TTC = 7.4 ± 0.4 
EC = 6.8
IE = 5.8
FC = 7.0
TC = 6.0
TTC = 6.7 
SC = 6.2 ± 0.3
RNA-F = 6.0 ± 0.4
BFP = 3.9 ± 1.7 
SC = 4.5
RNA-F = 5.8
BFP = 3.9 
De Luca et al. (2013)  EC = 6.0–7.9
IE = 5.5–6.3 
EC = 6.8
IE = 5.8 
SC = 5.0–6.8
RNA-F = 5.2–7.0 
SC = 4.3
RNA-F = 5.8 
Ottoson et al. (2006)  Sweden
(450 PE) 
EC = NA
IE = NA 
EC = 5.0 ± 0.9
IE = 4.5 ± 1.1 
RNA-F = NA
SC = NA
Cry = 0.7 ± 0.5
Gia = 3.1 ± 0.4 
RNA-F = 3.8 ± 0.9
SC = 3.1 ± 0.7
Cry = >1.4
Gia = >3.9 
Purnell et al. (2016)  United Kingdom (300,000 PE) IE = 6.0–6.5
FC = 6.7–7.2 
IE = 6.2
FC = 7.0 
SC = 5.5–6.5
RNA-F = 3.2–4.6 
SC = 5.6
RNA-F = 3.9 

PE, population equivalent; NA, not analyzed.

EC, Escherichia coli (in MPN or CFU/100 mL); IE, intestinal enterococci (in MPN or CFU/100 mL); TC, total coliforms (in CFU/100 mL); FC, faecal coliforms (in CFU/100 mL or CFU/mL); RNA-F, F-specific RNA phages (in PFU/100 mL or PFU/50 mL); SSR, spores of sulfite reducing bacteria (in CFU/100 mL); SC, somatic coliphages (in PFU/100 mL or PFU/mL); Cry, cryptosporidium (in (oo)cysts/L); Gia, Giardia (in (oo)cysts/L); MSC, male-specific coliphages (in PFU/100 mL); BFP, phages infecting Bacteroides fragilis (in PFU/100 mL).

Figure 1

Concentrations and removals of pathogen indicators in Parisian WWTPs based on activated sludge, biofiltration and MBR.

Figure 1

Concentrations and removals of pathogen indicators in Parisian WWTPs based on activated sludge, biofiltration and MBR.

In Parisian wastewaters, high concentrations of faecal bacteria are measured, with average concentrations of 6.9–7.3 log MPN/100 mL for EC and 6.0–6.5 log MPN/100 mL for IE respectively depending on the WWTP. The variability is relatively low for both indicators with variation coefficients of 4–12% for EC and 5–8% for IE. Significant differences were found between SAV or SEC or SEG and SEM or SEV, both for EC (Kruskal–Wallis test then pairwise comparison, p-values = 0.0001 to 0.04) and IE (Kruskal–Wallis test then pairwise comparison, p-values = <0.0001 to 0.002). These differences in raw wastewater between SEV/SEM and SAV/SEC are probably due to different sewage networks (SIAAP source), as SEV/SEM correspond to the eastern network (mix of combined and separate sewer networks, Supplementary Information – Table S1) and SAV/SEC to the western network (totally combined sewer network), which may result in differences of wastewater origin, dilution rates by rainfall or drained underground waters, and hydraulic retention time in sewers. These concentrations are comparable to those reported in the literature in wastewater for EC and overall in the upper range for IE (Table 1). In addition, no seasonal variations were observed both in concentrations and removals of pathogens.

The average EC removal achieved in Parisian WWTPs is 2.7–3.2 log in SAV, SEV, SEG and SEC, and significantly greater in SEM (Mann–Whitney test, p-value < 0.0001) with a value of 5.5 log. The average IE removal is 2.8–3.4 log except for SEM, which has a significantly greater removal of 4.7 log (Mann–Whitney test, p-value < 0.0001). Thus, the MBR WWTP (SEM) allows achievement of faecal bacteria removals 2.3–2.8 log greater than conventional activated sludge and biofiltration WWTPs, initial concentrations being comparable. In addition, SAV has significantly lower removals than the other WWTPs for both EC and IE (Mann–Whitney or Student tests, p-values = <0.0001 to 0.016), except for IE in SEV (Mann–Whitney test, p-value = 0.954). SEV has also a lower removal than SEG and SEC for IE (Mann–Whitney tests, p-values = <0.0001 to 0.013). Both SAV and SEV have slightly lower removal of TSS compared to the others, respectively 95.8 and 97.4% against 97.8–99.4%, which could explain those observations as faecal bacteria removals are significantly correlated to TSS removal in the studied WWTPs (Pearson test, p-value = 0.004 for EC and <0.0001 for IE). Regarding both biofiltration WWTPs (SEG and SEC), they have a significantly similar removal of EC (Student test, p-value = 0.747) but not for IE (Student test, p-value = 0.011) even if average values are close, i.e. 3.4 log in SEC and 3.1 log in SEG. It can be assumed that conventional activated sludge and biofiltration WWTPs have similar efficiencies to remove faecal bacteria when their physico-chemical performances are similar.

Data about the removals of faecal bacteria in full-scale WWTPs based on conventional activated sludge, biofiltration or MBR are scarce (only nine papers found) and synthetized in Table 1. This is particularly the case for biofiltration, with only the study from Dias et al. (2018), which reported lower removals than Parisian WWTPs, i.e. 1.9 log for IE and 1.7 log for faecal coliforms. This study is then the first to confirm a similar efficiency of biofiltration compared to conventional activated sludge regarding faecal bacteria. The lower removals reported by Dias et al. (2018) could be explained by a lower efficiency of those WWTPs regarding physico-chemical parameters but such information is not available in the paper except the fact that those WWTPs have small or medium sizes. For MBR, the four papers found about full-scale results indicate high removals of 4.5–7.0 log and similar to those in SEM. The removals observed in SEV are comparable to those reported in the literature for conventional activated sludge. They are in particular similar to Ottoson et al. (2006), Fu et al. (2010) and Dias et al. (2018), greater than Wen et al. (2009), De Luca et al. (2013), Dias et al. (2018) and lower than Zhang & Farahbakhsh (2007) and Montazeri et al. (2015). Data from Parisian WWTPs confirm the scarce data found in the literature for conventional activated sludge and MBR, at lager scale.

RNA-F bacteriophages and SSR fate in conventional activated sludge, biofiltration and MBR WWTPs

Compared with faecal bacteria, both other pathogen indicators have lower initial concentrations and a greater variability in Parisian raw wastewater. Indeed, RNA-F bacteriophages are found at between 3.2 and 4.0 log PFU/50 mL on average with variation coefficients between 25 and 36%. In particular, RNA-F bacteriophages are sometimes measured in raw wastewater below 2 log (n = 16), particularly in WWTPs from the western part of Paris, SAV (n = 4), SEC (n = 6) and SEG (n = 5). RNA-F concentrations are in the same order of magnitude in the different WWTPs and not significantly different in one WWTP compared to the other WWTPs (Kruskal–Wallis test, p-value = 0.226). SSR are found at between 3.9 and 4.9 log CFU/100 mL on average with variation coefficients between 6 and 21%. Concentrations are always higher than 2 log except for one campaign in SEM where SSR was not quantified. SSR concentrations are also in the same order of magnitude in the different WWTPs but significantly lower in SEV compared to the other WWTPs (Kruskal–Wallis test then pairwise comparison, p-value = <0.0001).

Data about both indicators are very scarce, in particular for SSR, as no publication was found about the fate of this indicator in WWTPs (Table 1). For RNA-F bacteriophages, the concentrations found in Parisian WWTPs are similar (Purnell et al. 2016; Dias et al. 2018) or lower than those reported in the literature (Ottoson et al. 2006; Zhang & Farahbakhsh 2007; Zanetti et al. 2010; De Luca et al. 2013). Low concentrations in raw wastewater are not favorable to the achievement of a high removal.

RNA-F bacteriophages are removed by between 0.9 and 3.1 log on average in the five studied WWTPs. Similarly to faecal bacteria, the removal is significantly higher in SEM compared to the other WWTPs (Mann–Whitney tests, p-values = <0.0001 to 0.014), being 1 log greater compared to SEV and 2 log greater compared to the others. In addition, Figure 1 displays a significantly (Mann–Whitney tests, p-values = <0.0001 to 0.0004) higher RNA-F removal of 1 log in the conventional activated sludge WWTP (SEV) compared to biofiltration WWTPs (SAV, SEG and SEG). Even if RNA-F concentration in raw wastewater is higher in SEV, this greater removal cannot be solely explained by this initial concentration difference. The higher hydraulic retention time in activated sludge processes compared to biofiltration could favor the mortality of those bacteriophages.

In the six papers found dealing with RNA-F fate in WWTPs, the removal of this indicator in SEM is similar to those reported in MBR (Ottoson et al. 2006; Zanetti et al. 2010; De Luca et al. 2013; Purnell et al. 2016), i.e. 3.8–5.8 log, the greater removals corresponding to higher initial concentrations. Similarly, the SEV removal is comparable to Dias et al. (2018), which reported similar initial concentrations of 3.3 log, but lower than the other papers (Ottoson et al. 2006; Zhang & Farahbakhsh 2007; De Luca et al. 2013), i.e. 3.1–5.5 log, which reported higher initial concentrations of 5.2–7.0 log. Finally, RNA-F removal reported by Dias et al. (2018) in a biofiltration WWTP is way lower than the one from Parisian WWTPs for comparable initial concentrations. The same hypothesis made for faecal bacteria could be made for RNA-F (lower efficiency regarding physico-chemical parameters).

Regarding SSR, the results presented in Figure 1 are to the authors' knowledge the first published about full-scale WWTPs based on conventional activated sludge, biofiltration or MBR. They indicate that SSR removals are between 1.2 and 3.7 log in Parisian WWTPs, the removal being 3.7 log significantly higher in SEM (Mann–Whitney tests, p-values = <0.0001). SEV is significantly less efficient for this indicator (Mann–Whitney tests, p-values = <0.0001 to 0.001), the removal of 1.2 log being the lowest compared to biofiltration WWTPs (1.5–1.9 log), but this is explained by a 1 log lower initial concentration. The different localization and sewer network characteristics (eastern Paris) could be an explanation for this lower concentration. Thus, it can be assumed that conventional activated sludge and biofiltration WWTPs have comparable efficiency regarding SSR when their physico-chemical parameters efficiency is similar.

Correlations between pathogen indicators and conventional water quality parameters

Statistical relationships between pathogen indicators and physico-chemical parameters were investigated to evaluate (1) the correlations between pathogen indicators in raw wastewater (RW), (2) the removal dependence on initial concentration, (3) the correlations between pathogen indicator removals and (4) the correlations between pathogen indicator removals and conventional parameters monitored on a daily basis (TSS, COD, N-NH4 and P-PO4) removals. The impact of hydraulic residence time was also investigated in SEV but no significant correlation was found between this parameter and pathogen removals (Spearman tests, p-value > 0.05). Table 2 synthetizes the results of those correlation tests, performed with XL Stat software. Pearson or Spearman tests were performed depending on the normality (Shapiro–Wilk test) of the series, using all data available from the five WWTPs. The number of values, n, is similar between a given pathogen indicator and its removal, as well as physico-chemical parameter removals as they are monitored on a daily basis.

Table 2

Correlations between pathogen indicator removals and physico-chemical parameters in the five Parisian WWTPs (significant correlations in bold)

EC removal
(n = 255 values)
EI removal
(n = 249 values)
RNA-F removal
(n = 102 values)
SSR removal
(n = 168 values)
Pathogen indicator concentration in RW rP = 0.463 rP = 0.393 rS = 0.547 rS = 0.533 
p = <0.0001 p = <0.0001 p = <0.0001 p = <0.0001 
EC removal  rP = 0.691 rS = 0.313 rS = 0.070 
p = <0.0001 p = 0.001 p = 0.367 
EI removal   rS = 0.023 rS = 0.331 
p = 0.824 p = <0.0001 
RNA-F removal    rS = −0.240 
p = 0.019 
TSS removal rP = 0.178 rP = 0.277 rS = 0.018 rS = 0.174 
p = 0.004 p = <0.0001 p = 0.856 p = 0.024 
COD removal rP = 0.117 rP = 0.184 rS = 0.311 rS = 0.061 
p = 0.063 p = 0.004 p = 0.002 p = 0.432 
N-NH4 removal rP = 0.149 rP = 0.207 rS = 0.293 rS = −0.010 
p = 0.017 p = 0.001 p = 0.003 p = 0.894 
P-PO4 removal rP = 0.057 rP = 0.206 rS = −0.165 rS = 0.125 
p = 0.419 p = 0.003 p = 0.140 p = 0.142 
EC removal
(n = 255 values)
EI removal
(n = 249 values)
RNA-F removal
(n = 102 values)
SSR removal
(n = 168 values)
Pathogen indicator concentration in RW rP = 0.463 rP = 0.393 rS = 0.547 rS = 0.533 
p = <0.0001 p = <0.0001 p = <0.0001 p = <0.0001 
EC removal  rP = 0.691 rS = 0.313 rS = 0.070 
p = <0.0001 p = 0.001 p = 0.367 
EI removal   rS = 0.023 rS = 0.331 
p = 0.824 p = <0.0001 
RNA-F removal    rS = −0.240 
p = 0.019 
TSS removal rP = 0.178 rP = 0.277 rS = 0.018 rS = 0.174 
p = 0.004 p = <0.0001 p = 0.856 p = 0.024 
COD removal rP = 0.117 rP = 0.184 rS = 0.311 rS = 0.061 
p = 0.063 p = 0.004 p = 0.002 p = 0.432 
N-NH4 removal rP = 0.149 rP = 0.207 rS = 0.293 rS = −0.010 
p = 0.017 p = 0.001 p = 0.003 p = 0.894 
P-PO4 removal rP = 0.057 rP = 0.206 rS = −0.165 rS = 0.125 
p = 0.419 p = 0.003 p = 0.140 p = 0.142 

RW, raw wastewater.

rP, Pearson coefficient of correlation; rS, Spearman coefficient of correlation.

In RW, logically, a significant relationship was found between EC and IE concentrations (Pearson test, r = 0.495, p-value < 0.0001), but also between IE and SSR even if the correlation is not good (Pearson test, r = −0.174, p-value = 0.018). No statistical relationships were found between EC, SSR and RNA-F, and between IE and RNA-F (Pearson test, p-values > 0.05). Regarding the dependence of pathogen indicator removals to the initial concentrations in RW (Table 2), significant correlations were found for the four pathogens, confirming that removals increase with the initial concentration, so low initial concentrations are unfavorable to high removals in those types of WWTPs. Correlations are better for RNA-F and SSR, with correlation coefficients higher than 0.5. Regarding the correlations between the different pathogens' fate, IE and EC removals are significantly correlated with a moderate correlation coefficient. RNA-F removal is significantly correlated to EC and SSR removals but not to IE removal, while SSR removal is also correlated to IE but not EC. This would confirm that improving the removal of faecal bacteria within such biological treatments would also improve the removal of RNA-F and SSR, even if their removals are lower. Removals of pathogen indicators are significantly correlated to the WWTP efficiency regarding physico-chemical parameters. TSS and N-NH4 removals are correlated to both EC and IE removals, and TSS is also significantly correlated to SSR removal while N-NH4 is correlated to RNA-F removal. Dissolved organic carbon (DOC) could also be a surrogate of IE and RNA-F, while P-PO4 is correlated only to IE removal. This would indicate that TSS, DOC or N-NH4 could be used as surrogates of pathogen indicator fate but the correlations are not good enough to allow good predictions. A very high physico-chemical level of treatment is required to eliminate pathogen indicators in conventional WWTPs but not sufficient to guarantee the compliance with reuse guidelines.

Efficiency of tertiary treatments to remove pathogen indicators

Figure 2 synthetizes the results obtained in Parisian WWTPs of SEC and SEV within the study of tertiary treatment implementation for micropollutants removal, a fluidized bed micro-grain activated carbon (μGAC) process (Mailler et al. 2015, 2016; Guillossou et al. 2019), ozonation (Guillossou et al. 2020), or faecal bacteria disinfection by performic acid (PFA). For each technology, the pathogen indicator removals were determined within the following configurations: 10 g/m3 fresh μGAC injection (20 minutes contact time), 0.9–1.3 g O3/g DOC for ozonation (10 minutes contact time) and 0.9–1.2 ppm of PFA (10–20 minutes contact time).

Figure 2

Removal of pathogens in WWTP discharge by micro-grain activated carbon (µGAC), ozonation and performic acid (PFA) disinfection.

Figure 2

Removal of pathogens in WWTP discharge by micro-grain activated carbon (µGAC), ozonation and performic acid (PFA) disinfection.

The μGAC process operating with a fresh μGAC injection of 10 g/m3 and applied to SEC discharge resulted in a decrease of 0.8 ± 0.4 log for EC and 0.8 ± 0.2 log for IE. These removals were achieved with initial concentrations of 4.7 ± 0.6 log MPN/100 mL for EC and 3.0 ± 0.1 log MPN/100 mL for IE. Rather than by adsorption, it could be explained by the filtration effect of the fluidized bed leading to the retention of TSS (Mailler et al. 2016; Guillossou et al. 2019). If this is the case, faecal bacteria removals could be higher in other WWTPs with higher TSS concentrations as TSS concentration in SEC WWTP is very low (3 ± 2 mg/L on average in 2014–2018). For SSR, a negligible removal is observed and it can be considered that this process has no effect on this parameter. For RNA-F, no removal could be determined as the initial concentrations were always below the LQ. No paper was found in the literature about pathogen indicator fate within activated carbon processes.

Ozonation operated at 0.9–1.3 g O3/g DOC and applied to SEC nitrified water led to good removals for the four indicators. Such ozone doses are in the upper range of what is currently recommended for micropollutants removal (0.4–0.7 g O3/g DOC) in Switzerland (Bourgin et al. 2018). The best removal is obtained for EC with an average of 1.7 ± 0.2 log while IE, RNA-F and SSR have comparable removals of 1.0–1.1 log. These removals were achieved with initial concentrations of 4.2 ± 0.2 log MPN/100 mL for EC, 2.4 ± 0.2 log MPN/100 mL for IE, 1.9 ± 0.4 CFU/100 mL for RNA-F and 3.2 ± 0.5 PFU/50 mL for SSR. EC and SSR were quantified in every ozonized water sample, while IE and RNA-F were not quantified (<LQ) in all cases, so the reported removals are underestimated as calculated using LQ as the concentration in treated water. Higher removals could then be achieved by the application of higher ozone specific doses in the case of water with higher initial concentrations. Ozone disinfection efficiency is well established in the literature. Lazarova et al. (2013) indicated that a transferred ozone dose of 6–17 mgO3/L is required to achieve a 2 log removal of faecal coliforms in biologically treated wastewater, and higher doses allow an increase in the bacteria removals. Similarly, Liberti et al. (2000) reported 2.5–3 log removals of total coliforms from a biologically treated wastewater, while Mezzanotte et al. (2007) indicated higher removals of around 4 log for EC and faecal coliforms for transferred ozone doses lower than 10 mgO3/L. However, production of disinfection by-products has to be evaluated in the case of ozonation, which was not the case in our study.

PFA disinfection, operated at 0.9–1.2 ppm and applied to SEV discharge at laboratory scale (9–12 ppm·min), led to high faecal bacteria removals of 2.6 ± 0.7 log for EC and 1.7 ± 0.7 log for IE. At industrial scale (10–30 ppm·min), the removals were 1.9 ± 0.7 log for EC and 1.8 ± 0.7 log for IE. Regarding RNA-F and SSR, removals of around 0.8 log were observed at laboratory or industrial scale. PFA efficiency to disinfect treated wastewater has been reported in the literature. Full-scale removals of 1 and 0.5–2 log respectively for EC and IE at 4–5 ppm·min (Karpova et al. 2013), 3.3 and 2.5 log at 15 ppm·min (Luukkonen et al. 2015) or 2–4.2 and 0.7–3.2 log at 23 ppm·min (Ragazzo et al. 2013) were reported. Data about bacteriophages are very scarce but (Karpova et al. 2013) observed a removal of 4 log of somatic coliphages at 10 ppm·min in treated wastewater, while (Gehr et al. 2009) published removals of RNA-F bacteriophages from settled wastewater of 1–2 log at very high PFA cumulated dose (concentration × time) of 450–540 ppm·min. The SSR data presented in this study are the first published to the authors’ knowledge.

Discussion about the treated wastewater reuse potential in the Paris area

Data were compared to the French wastewater reuse regulation (Arrêté du 25 juin 2014); 88% (SAV) to 100% (SEM) of the TSS and COD data are in compliance with the category A (strictest quality standards) of the regulation within the nominal operation of the five Parisian WWTPs, and 95% (SAV) to 100% (SEM) of them satisfy the criteria for category B. Physico-chemical parameters are then not problematic in Paris for wastewater reuse. For pathogen indicators, there is a clear difference between the MBR WWTP (SEM) and the other ones. For SEM (MBR), 99% of the values for EC and 97% for IE comply with the category A, while the quality complies with categories C or D (least strict quality standards) 97% of the time for SSR and 93% of the time for RNA-F bacteriophages. SEM is then compatible with reuse without a disinfection treatment. For the other WWTPs, based on conventional activated sludge or biofiltration, the treated wastewater quality complies with the categories C or D less than 50% of the time due to SSR or RNA-F bacteriophages. RNA-F bacteriophages removals in SEV are sufficient to reach the categories C or D for this parameter 68% of the time, against 5–14% for biofiltration facilities. For SSR, 6% (SEV) to 38% (SEG) of the calculated removals are sufficient for categories C or D. However, those WWTPs have high compliance rates with categories C or D for faecal bacteria, 81–100% for EC and 88–98% for IE.

As previously demonstrated, the calculated removals of pathogen indicators within the five WWTPs are correlated to initial concentrations in raw wastewater. In theory, the calculated removal can be low or not sufficient regarding wastewater reuse for two very different reasons: (1) the pathogen indicator is still quantified above the LQ in the treated wastewater, which means that the process is not efficient enough, or (2) the pathogen is not quantified in the WWTP outlet (<LQ), which means that the calculated removal is an underestimation of the reality. To investigate this point, time evolutions of SSR and RNA-F bacteriophages concentrations were plotted in Figure 3. The same plots are available for EC and IE in Supplementary Information – Figure S2. The minimal concentrations required in raw wastewater to calculate a removal of 2 log considering the LQ of the analytical methods employed in this paper, and using LQ value as final value, are represented in Figure 3. The LQ values are as follows: 1.18 log MPN/100 mL for EC and IE, 0 log PFU/50 mL for RNA-F bacteriophages and 0 log CFU/100 mL for SSR. So the minimal concentrations required to calculate a 2 log removal (reuse quality categories C or D) are 3.18 log for EC and IE and 2 log for RNA-F bacteriophages and SSR. The time evolutions of the four pathogens' removals are given in the Supplementary Information – Figure S3.

Figure 3

Evolution of SSR and RNA-F bacteriophage concentrations in raw wastewater in the five Parisian WWTPs from 2014 to 2018.

Figure 3

Evolution of SSR and RNA-F bacteriophage concentrations in raw wastewater in the five Parisian WWTPs from 2014 to 2018.

Two types of trends are observable within the four pathogen indicators of the reuse regulation. First, EC, IE and SSR concentrations in Parisian raw wastewater are relatively stable in time between 2014 and 2018, even if some differences can be observed from one WWTP to another. Thus, EC and IE concentrations vary around 7 and 6 log respectively, while SSR concentration varies around 5 log. In contrast, a clear temporal evolution is observed for RNA-F bacteriophages with a decrease of concentration in Parisian raw wastewater from 2017, except in the case of SEM. RNA-F bacteriophages concentrations measured between 2017 and 2018 in SAV, SEV, SEG and SEC raw wastewater are significantly lower than those from 2014 to 2016 (Mann–Whitney test, p-value < 0.0001). This significant trend is surprising and no technical explanations could be found regarding SIAAP operation of the network. In addition, the sampling and analysis methodology were strictly similar during the whole period.

Moreover, the discrepancy between RNA-F bacteriophages and the other pathogen indicators is confirmed when comparing the measured concentrations to the minimum required to be able to calculate a 2 log removal when reaching LQ in treated wastewater. In fact, in contrast to EC, IE and SSR, which always have higher concentrations than this limit, RNA-F bacteriophages are frequently measured below this limit from 2017 (n = 16). Thus, low SSR removals observed in Parisian WWTPs correspond to an insufficient efficiency of conventional activated sludge and biofiltration with a lack of 0.5–1.0 log most of the time. In contrast, there is a real technical problem with RNA-F bacteriophages to evaluate the compliance with the reuse regulation. The modification of the regulation to consider this issue would be necessary to indicate a minimum removal of 2 log or a concentration in the treated wastewater below 1 PFU/50 mL. When focusing on 2014–2016, it is nevertheless possible to highlight that SEV removes more than 2 log of this indicator most of the time, while removals in the biofiltration WWTPs are still lower than 2 log. This would indicate that conventional activated sludge WWTPs are more efficient than biofiltration WWTPs regarding RNA-F bacteriophages removal, when the initial concentration is high enough. This could be explained by the notably higher hydraulic retention time in conventional activated sludge (≈8 h) compared to biofiltration units (<2 h).

CONCLUSIONS

This study investigated the fate of the four pathogen indicators used in the French reuse regulation (EC, IE, RNA-F bacteriophages and SSR) within five large-scale Parisian WWTPs, based on conventional activated sludge, biofiltration or MBR technology. Removals of 3 log for both EC and IE, and lower removals of 1–2 log for SSR and RNA-F bacteriophages were observed in conventional activated sludge and biofiltration WWTPs. The MBR WWTP had the greatest removals for each of the indicators, respectively 4.5–5.5 log for faecal bacteria and 3–4 log for SSR and RNA-F bacteriophages, and was the only one to comply with reuse standards more than 90% of the time. For the other WWTPs, the implementation of a tertiary treatment would be necessary. Within the three technologies studied in Parisian wastewaters, µGAC demonstrated a significant reduction of faecal bacteria concentrations of 0.8 log and no effect on SSR and bacteriophages. Ozone and PFA at reasonable doses demonstrated high supplementary removals of 1.5–2.5 log for EC, 1.0–2.0 log for IE, and 0.5–1.0 log for SSR and RNA-F bacteriophages. The removals of pathogen indicators were significantly correlated to their initial concentrations in raw wastewater, which were low compared to the scarce literature for RNA-F bacteriophages. In fact, a clear and unexplained decrease of concentration was observed in the Parisian wastewater for this indicator from summer 2017, leading to concentrations frequently below 2 log, which is the minimum removal required for reuse. In consequence, this parameter is regularly not quantified in the treated wastewater (<LQ). This parameter is clearly an issue regarding the current reuse regulation and clarifications are needed, in particular for the evaluation of reuse compliance when it is not quantified in treated wastewater. Nevertheless, SSR had high initial concentrations (5 log) and low removals in Parisian WWTPs. It can be concluded that this indicator is the most difficult to remove from wastewater, even with tertiary oxidative treatments, and will drive the reuse of treated wastewater in Paris. Finally, significant correlations were found between the four pathogen indicator removals and TSS, COD, P-PO4 or N-NH4 removal, but they were not good, preventing performance predictions based on them. However, this highlights that a very efficient treatment of physico-chemical parameters of wastewater is required but not sufficient to comply with the reuse regulation.

ACKNOWLEDGEMENT

Authors would like to acknowledge all the SIAAP teams that participated to sampling and analyses, including SAV, SEV, SEG, SEC and SEM operators and SIAAP central laboratory.

DATA AVAILABILITY STATEMENT

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

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Supplementary data