Removal of MS2, Qb and GA bacteriophages during drinking water treatment at pilot scale Nicolas Boudaud a, *, Claire Machinal a , Fabienne David a , Armelle Fre ´val-Le Bourdonnec a , Je ´ro ˆme Jossent a , Fanny Bakanga a , Charlotte Arnal a , Marie Pierre Jaffrezic a , Sandrine Oberti a , Christophe Gantzer b a Veolia Environment Research and Innovation, Chemin de la Digue, BP76, 78608 Maisons-Laffitte Cedex, France b Laboratoire de Chimie Physique et Microbiologie pour l’Environnement (LCPME), Nancy Universite ´/CNRS, Faculte ´ de Pharmacie, 5 rue Albert Lebrun, 54000 Nancy, France article info Article history: Received 1 March 2011 Received in revised form 27 January 2012 Accepted 11 February 2012 Available online xxx Keywords: Bacteriophages Virus removal Drinking water Treatment Clarification Filtration Chlorine disinfection abstract The removal of MS2, Qb and GA, F-specific RNA bacteriophages, potential surrogates for pathogenic waterborne viruses, was investigated during a conventional drinking water treatment at pilot scale by using river water, artificially and independently spiked with these bacteriophages. The objective of this work is to develop a standard system for assessing the effectiveness of drinking water plants with respect to the removal of MS2, Qb and GA bacteriophages by a conventional pre-treatment process (coagulation–flocculation– settling-sand filtration) followed or not by an ultrafiltration (UF) membrane (complete treatment process). The specific performances of three UF membranes alone were assessed by using (i) pre-treated water and (ii) 0.1 mM sterile phosphate buffer solution (PBS), spiked with bacteriophages. These UF membranes tested in this work were designed for drinking water treatment market and were also selected for research purpose. The hypothesis serving as base for this study was that the interfacial properties for these three bacteriophages, in terms of electrostatic charge and the degree of hydropho- bicity, could induce variations in the removal performances achieved by drinking water treatments. The comparison of the results showed a similar behaviour for both MS2 and Qb surrogates whereas it was particularly atypical for the GA surrogate. The infectious char- acter of MS2 and Qb bacteriophages was mostly removed after clarification followed by sand filtration processes (more than a 4.8-log reduction) while genomic copies were removed at more than a 4.0-log after the complete treatment process. On the contrary, GA bacteriophage was only slightly removed by clarification followed by sand filtration, with less than1.7-log and 1.2-log reduction, respectively. After the complete treatment process achieved, GA bacteriophage was removed with less than 2.2-log and 1.6-log reduction, respectively. The effectiveness of the three UF membranes tested in terms of bacteriophages removal showed significant differences, especially for GA bacteriophage. These results could provide recommendations for drinking water suppliers in terms of selection criteria for membranes. MS2 bacteriophage is widely used as a surrogate for pathogenic waterborne viruses in Europe and the United States. In this study, the choice of MS2 bacteriophage as the best * Corresponding author. Tel.: þ33 1 34 93 31 87; fax: þ33 1 34 93 31 10. E-mail address: [email protected](N. Boudaud). Available online at www.sciencedirect.com journal homepage: www.elsevier.com/locate/watres water research xxx (2012) 1 e14 Please cite this article in press as: Boudaud, N., et al., Removal of MS2, Qb and GA bacteriophages during drinking water treatment at pilot scale, Water Research (2012), doi:10.1016/j.watres.2012.02.020 0043-1354/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2012.02.020
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wat e r r e s e a r c h x x x ( 2 0 1 2 ) 1e1 4
Available online at w
journal homepage: www.elsevier .com/locate/watres
Removal of MS2, Qb and GA bacteriophages during drinkingwater treatment at pilot scale
Nicolas Boudaud a,*, Claire Machinal a, Fabienne David a, Armelle Freval-Le Bourdonnec a,Jerome Jossent a, Fanny Bakanga a, Charlotte Arnal a, Marie Pierre Jaffrezic a,Sandrine Oberti a, Christophe Gantzer b
aVeolia Environment Research and Innovation, Chemin de la Digue, BP76, 78608 Maisons-Laffitte Cedex, Franceb Laboratoire de Chimie Physique et Microbiologie pour l’Environnement (LCPME), Nancy Universite/CNRS, Faculte de Pharmacie,
treatment process (Table 3). On the other hand, overall GA
bacteriophage removal was around 1.3e1.6-log reduction
after the pre-treatment process followed by the UF A
treatment.
Chlorine disinfection is widely used in drinking water
plants prior to distribution. Thus, in order to ensure secure
processes for drinking water based on the GA model (>4.0-log
reduction), kinetics of inactivation and removal of GA andMS2
bacteriophages by residual chlorine were performed (Fig. 6).
An initial chlorine concentration of 1.5 mg/L was injected into
the permeate after UF of the pre-treated water to obtain
a residual chlorine concentration of about 0.3 mg/L after
a contact time of 5 min. The sharp drop in residual chlorine
between 0 and 2minwas due to oxidation of NOM found in the
permeate, generating chlorination by-products with less
activity than residual chlorine.
Inactivation kinetics showed a rapid decrease of infectious
GA and MS2 bacteriophage concentrations during the first
2 min of contact time (w3.0-log and 4.8-log reduction,
respectively) (Fig. 6a). Logarithmic reduction of phage
concentrations was then slower because residual chlorine
concentration ranged around 0.3e0.4 mg/L. Within this
resource, MS2 bacteriophage appeared more sensitive to
residual chlorine than GA bacteriophage at equivalent contact
times. This result was confirmed by the kinetics of removal of
total GA and MS2 bacteriophages, although the decrease in
genomic RNA concentrationwas slower for both phages under
the same conditions (Fig. 6b). After a contact time of 60 min,
total GA and MS2 bacteriophage concentrations were 1.86-log
and 0.55-log particles/mL, respectively. The lowest loga-
rithmic reduction of total bacteriophages compared to infec-
tious bacteriophages is due to the sequential action of residual
chlorine which first affects the phage capsid integrity before
to degrade genomic RNA (Nuanualsuwan and Cliver, 2002;
Cliver, 2009).
MS2 bacteriophage higher sensitivity to residual chlorine
was unexpected since this disinfectant induces non-specific
oxidative damages against bacteriophages. Therefore, the
same disinfection tests were repeated on demineralizedwater
spiked to about 106 PFU/mL with either GA or MS2 bacterio-
phages. In order to determine residual chlorine effectiveness,
Ct4log values were calculated for both bacteriophages in both
resource types. In demineralized water, the results showed
that residual chlorine was indeed inactivating GA and MS2
bacteriophages in a non-specific way since Ct4log were similar,
with 1.1 and 1.5 mg min L-1, respectively. On the other hand,
Ct4log values for the permeate produced by the drinking water
treatment pilot were much higher, with a difference of
0.8 mg min L-1 between GA (7.0 mg min L-1) and MS2 bacte-
riophages (6.2 mg min L-1). This result suggests that permeate
NOM could impact on the effectiveness of GA and MS2 inac-
tivation during the disinfection tests.
Residual chlorine doses typically used in drinking water
plants classically operated by Veolia Water are usually tar-
geted at 0.3 mg/L for 30 min, i.e. an actual Ct of 9.0 mgmin L-1.
Insofar as the calculated Ct4log for GA bacteriophage are lower
than the actual Ct implemented in drinking water plants,
these plants can be considered as safe with respect to the viral
risk based on the GA model (>4-log viral reduction
guaranteed).
Please cite this article in press as: Boudaud, N., et al., Removatreatment at pilot scale, Water Research (2012), doi:10.1016/j.wat
4. Conclusions
This study qualitatively and quantitatively assessed resis-
tance of MS2, GA and Qb bacteriophages towards surface
water treatments at pilot scale (clarification, sand filtration
andUF processes) representative of drinkingwater production
plants. The results indicated that MS2 and Qb bacteriophages
had a same behaviour during the application of the treatment
physical barriers, while GA displayed distinctive features.
Infectious and total bacteriophage logarithmic reductions for
MS2 and Qbwere above or equal to 4.0-log after the raw water
pre-treatment process and the UF membrane A (complete
treatment process), but under 2.2 and 1.6-log, respectively, in
the case of GA. Regarding GA bacteriophage, a chlorine
disinfection step after the complete treatment process ensure
the safety of drinking water plants in the conditions tested
(>4.0-log reduction).
Comparison of removal bacteriophages by the three UF
membranes tested, designed for drinking water treatment
market and actually used for research purpose, showed
specific relationship between membrane cutoff, electrostatic
interactions and hydrophobic properties, especially for GA
bacteriophage. This assessment of membrane performances
could provide recommendations for drinking water suppliers
in terms of selection criteria for membranes.
In the context of the assays undertaken at pilot scale, all
the results suggest that GA bacteriophage might be a more
suitable model for assessing the performance of drinking
water treatment processes in removing enteric viruses in
worst conditions than MS2, which is currently considered as
the reference model in the literature.
Further research is underway (i) to evaluate the effective-
ness of GA bacteriophage removal by other drinking water
treatments and (ii) to improve the knowledge on bacterio-
phage interfacial properties in relation to UF membrane-
based treatments.
Acknowledgements
This work was supported by Program grant ANR-07-PNRA-008
(ADHERESIST) from the ANR (Agence Nationale de la
Recherche).
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