Real-Time Online Monitoring for Assessing Removal of Bacteria by Reverse Osmosis
- Takahiro Fujioka*Takahiro Fujioka*E-mail: [email protected]. Telephone: +81 095 819 2695. Fax: +81 95 819 2620.Water and Environmental Engineering, Graduate School of Engineering, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, JapanMore by Takahiro Fujioka
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- Anh T. HoangAnh T. HoangWater and Environmental Engineering, Graduate School of Engineering, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, JapanMore by Anh T. Hoang
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- Hidenobu AizawaHidenobu AizawaEnvironment Management Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 16-1 Onogawa, Tsukuba, Ibaraki 305-8569, JapanMore by Hidenobu Aizawa
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- Hiroki AshibaHiroki AshibaElectronics and Photonics Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 5, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, JapanMore by Hiroki Ashiba
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- Makoto FujimakiMakoto FujimakiElectronics and Photonics Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 5, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, JapanMore by Makoto Fujimaki
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- Menu LeddyMenu LeddyOrange County Water District, 18700 Ward Street, Fountain Valley, California 92708, United StatesMore by Menu Leddy
Abstract

Rigorous monitoring of microbial water quality is essential to ensure the safety of recycled water after advanced treatment for indirect and direct potable reuse. This study evaluated real-time bacterial monitoring for assessing reverse osmosis (RO) treatment for removal of bacteria. A strategy was employed to monitor bacterial counts online and in real time in the RO feed and permeate water using a real-time continuous bacteriological counter. Over the course of 68 h pilot-scale testing, bacterial counts were monitored in real time over approximate ranges from 1 × 103 to 4 × 104 and from 4 to 342 counts/mL in the RO feed (ultrafiltration-treated wastewater) and permeate, respectively. The results indicate that the bacteriological counter can track the variations in bacterial counts in the RO feed and permeate. Bacterial concentrations were confirmed by epi-fluorescence microscopy for total bacterial counts. A high correlation (R2 = 0.83) was identified between the online bacterial counts and epi-fluorescence counts in the RO feed; a negligible correlation was observed for RO permeate. In this study, we evaluated a real-time bacteriological counter (i.e., counts per milliliter every second) to ensure continuous removal of bacterial contaminants by RO treatment.
Introduction
Materials and Methods
Analytical Techniques
Validation Protocol
Results and Discussion
Real-Time Bacteriological Monitoring
Figure 1

Figure 1. EEM fluorescence spectrum of UF-treated wastewater (a) without dilution and (b) with a 25-fold dilution.
Figure 2

Figure 2. RO treatment of the UF-treated wastewater at a pilot scale: (a) conductivity, (b) online-monitored bacterial counts (plotted every 10 min), and (c) total bacterial counts (determined by epi-fluorescence). The RO feed temperature was maintained at 14–16 °C (Figure S3).
Figure 3

Figure 3. Total bacterial count (determined by epi-fluorescence) as a function of online bacterial count during RO treatment of the UF-treated wastewater.
Passage of Bacteria through the RO Membrane
Implications for On-Site Use
Supporting Information
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.estlett.8b00200.
Additional text and figures (PDF)
Terms & Conditions
Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.
Acknowledgments
The authors acknowledge Hydranautics for providing RO membrane elements. The authors also acknowledge Azbil Corp. for providing real-time bacteriological monitors.
References
This article references 29 other publications.
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- 27Laurent, P.; Servais, P.; Gatel, D.; Randon, G.; Bonne, P.; Cavard, J. Microbiological quality: Before and after nanofiltration. J. - Am. Water Works Assoc. 1999, 91 (10), 62– 72, DOI: 10.1002/j.1551-8833.1999.tb08716.xGoogle Scholar27https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADyaK1MXmslOrur4%253D&md5=b2aa68eb9a35ed9dee6bc8f496b2dadcMicrobiological quality before and after nanofiltrationLaurent, Patrick; Servais, Pierre; Gatel, Dominique; Randon, Guy; Bonne, Pascal; Cavard, JacquesJournal - American Water Works Association (1999), 91 (10), 62-72CODEN: JAWWA5; ISSN:0003-150X. (American Water Works Association)The authors investigated microbiol. behavior of a distribution system supplied initially with biol. treated water and then with nanofiltered water. Their purpose was to identify and evaluate the changes in microbiol. water quality attributable to modifications in water treatment at the plant. During the course of the study, all data from various indicators of microbiol. quality (i.e., heterotrophic plate counts, coliform enumeration, total direct counts, and fixed bacterial biomass) showed similar trends. Results indicated that the use of nanofiltration allows utilities to reduce chlorination of treated water and at least maintain or increase the microbiol. quality of distributed water for areas with high residence times.
- 28Pype, M.-L.; Lawrence, M. G.; Keller, J.; Gernjak, W. Reverse osmosis integrity monitoring in water reuse: The challenge to verify virus removal – A review. Water Res. 2016, 98, 384– 395, DOI: 10.1016/j.watres.2016.04.040Google Scholar28https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XnvFSjsbw%253D&md5=f397be33b159a97d02ccfce38be68652Reverse osmosis integrity monitoring in water reuse: The challenge to verify virus removal - A reviewPype, Marie-Laure; Lawrence, Michael G.; Keller, Jurg; Gernjak, WolfgangWater Research (2016), 98 (), 384-395CODEN: WATRAG; ISSN:0043-1354. (Elsevier Ltd.)A review with many refs. A reverse osmosis (RO) process is often included in the treatment train to produce high quality reuse water from treated effluent for potable purposes because of its high removal efficiency for salinity and many inorg. and org. contaminants, and importantly, it also provides an excellent barrier for pathogens. In order to ensure the continued protection of public health from pathogen contamination, monitoring RO process integrity is necessary. Due to their small sizes, viruses are the most difficult class of pathogens to be removed in phys. sepn. processes and therefore often considered the most challenging pathogen to monitor. To-date, there is a gap between the current log credit assigned to this process (detd. by integrity testing approved by regulators) and its actual log removal capability as proven in a variety of lab. and pilot studies. Hence, there is a challenge to establish a methodol. that more closely links to the theor. performance. In this review, after introducing the notion of risk management in water reuse, we provide an overview of existing and potentially new RO integrity monitoring techniques, highlight their strengths and drawbacks, and debate their applicability to full-scale treatment plants, which open to future research opportunities.
- 29Liu, G.; Lut, M. C.; Verberk, J. Q. J. C.; Van Dijk, J. C. A comparison of additional treatment processes to limit particle accumulation and microbial growth during drinking water distribution. Water Res. 2013, 47 (8), 2719– 2728, DOI: 10.1016/j.watres.2013.02.035Google ScholarThere is no corresponding record for this reference.
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Abstract
Figure 1
Figure 1. EEM fluorescence spectrum of UF-treated wastewater (a) without dilution and (b) with a 25-fold dilution.
Figure 2
Figure 2. RO treatment of the UF-treated wastewater at a pilot scale: (a) conductivity, (b) online-monitored bacterial counts (plotted every 10 min), and (c) total bacterial counts (determined by epi-fluorescence). The RO feed temperature was maintained at 14–16 °C (Figure S3).
Figure 3
Figure 3. Total bacterial count (determined by epi-fluorescence) as a function of online bacterial count during RO treatment of the UF-treated wastewater.
References
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- 17Fujioka, T.; Kodamatani, H.; Aizawa, H.; Gray, S.; Ishida, K. P.; Nghiem, L. D. Role of membrane fouling substances on the rejection of N-nitrosamines by reverse osmosis. Water Res. 2017, 118, 187– 195, DOI: 10.1016/j.watres.2017.03.057Google ScholarThere is no corresponding record for this reference.
- 18Liu, T.; Chen, Z.-l.; Yu, W.-z.; You, S.-j. Characterization of organic membrane foulants in a submerged membrane bioreactor with pre-ozonation using three-dimensional excitation–emission matrix fluorescence spectroscopy. Water Res. 2011, 45 (5), 2111– 2121, DOI: 10.1016/j.watres.2010.12.023Google Scholar18https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3MXitFaqurY%253D&md5=d8862c5f758d9b4d58f6d80045804e9dCharacterization of organic membrane foulants in a submerged membrane bioreactor with pre-ozonation using three-dimensional excitation-emission matrix fluorescence spectroscopyLiu, Ting; Chen, Zhong-lin; Yu, Wen-zheng; You, Shi-jieWater Research (2011), 45 (5), 2111-2121CODEN: WATRAG; ISSN:0043-1354. (Elsevier B.V.)This study focuses on org. membrane foulants in a submerged membrane bioreactor (MBR) process with pre-ozonation compared to an individual MBR using three-dimensional excitation-emission matrix (EEM) fluorescence spectroscopy. While the influent was continuously ozonated at a normal dosage, preferable org. matter removal was achieved in subsequent MBR, and trans-membrane pressure increased at a much lower rate than that of the individual MBR. EEM fluorescence spectroscopy was employed to characterize the dissolved org. matter (DOM) samples, extracellular polymeric substance (EPS) samples and membrane foulants. Four main peaks could be identified from the EEM fluorescence spectra of the DOM samples in both MBRs. Two peaks were assocd. with the protein-like fluorophores, and the other ones were related to the humic-like fluorophores. The results indicated that pre-ozonation decreased fluorescence intensities of all peaks in the EEM spectra of influent DOM esp. for protein-like substances and caused red shifts of all fluorescence peaks to different extents. The peak intensities of the protein-like substances represented by Peak T1 and T2 in EPS spectra were obviously decreased as a result of pre-ozonation. Both external and internal fouling could be effectively mitigated by the pre-ozonation. The most primary component of external foulants was humic acid-like substance (Peak C) in the MBR with pre-ozonation and protein-like substance (Peak T1) in the individual MBR, resp. The content decrease of protein-like substances and structural change of humic-like substances were obsd. in external foulants from EEM fluorescence spectra due to pre-ozonation. However, it could be seen that ozonation resulted in significant redn. of intensities but little location shift of all peaks in EEM fluorescence spectra of internal foulants.
- 19Nam, S.-N.; Amy, G. Differentiation of wastewater effluent organic matter (EfOM) from natural organic matter (NOM) using multiple analytical techniques. Water Sci. Technol. 2008, 57 (7), 1009– 1015, DOI: 10.2166/wst.2008.165Google Scholar19https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1cXntV2hur4%253D&md5=c2a8cd6adfeba15b5f966ab8615ee576Differentiation of wastewater effluent organic matter (EfOM) from natural organic matter (NOM) using multiple analytical techniquesNam, Seong-Nam; Amy, GaryWater Science and Technology (2008), 57 (7), 1009-1015CODEN: WSTED4; ISSN:0273-1223. (IWA Publishing)Using three anal. techniques of size exclusion chromatog. (SEC), fluorescence excitation-emission matrix (EEM), and dissolved org. nitrogen (DON) measurement, differentiating characteristics of effluent org. matter (EfOM) from natural org. matter (NOM) have been investigated. SEC reveals a wide range of mol. wt. (MW) for EfOM and high amt. of high MW polysaccharides, and low MW org. acids compared to NOM. Clear protein-like peaks using fluorescence EEM were a major feature of EfOM distinguishing it from NOM. Fluorescence index (FI), an indicator to distinguish autochthonous origin from allochthonous origin, differentiated EfOM from NOM by exhibiting higher values, indicating a microbial origin. In EfOM samples, DON present in higher amts. than NOM.
- 20Chen, W.; Westerhoff, P.; Leenheer, J. A.; Booksh, K. Fluorescence excitation–emission matrix regional integration to quantify spectra for dissolved organic matter. Environ. Sci. Technol. 2003, 37 (24), 5701– 5710, DOI: 10.1021/es034354cGoogle Scholar20https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD3sXovFeisrc%253D&md5=6fc1ca4c33117f277bf6d01dd21c9f5fFluorescence Excitation-Emission Matrix Regional Integration to Quantify Spectra for Dissolved Organic MatterChen, Wen; Westerhoff, Paul; Leenheer, Jerry A.; Booksh, KarlEnvironmental Science and Technology (2003), 37 (24), 5701-5710CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)Excitation-emission matrix (EEM) fluorescence spectroscopy has been widely used to characterize dissolved org. matter (DOM) in water and soil. However, interpreting the >10,000 wavelength-dependent fluorescence intensity data points represented in EEMs has posed a significant challenge. Fluorescence regional integration, a quant. technique that integrates the vol. beneath an EEM, was developed to analyze EEMs. EEMs were delineated into five excitation-emission regions based on the fluorescence of model compds., DOM fractions, and marine waters or fresh waters. Volumetric integration under the EEM within each region, normalized to the projected excitation-emission area within that region and dissolved org. carbon concn., resulted in a normalized region-specific EEM vol. (Φi,n). Solid-state carbon NMR (13C NMR), Fourier transform IR (FTIR) anal., UV-visible absorption spectra, and EEMs were obtained for std. Suwannee River fulvic acid and 15 hydrophobic or hydrophilic acid, neutral, and base DOM fractions plus nonfractionated DOM from wastewater effluents and rivers in the southwestern USA. DOM fractions fluoresced in one or more EEM regions. The highest cumulative EEM vol. (ΦT,n = ΣΦi,n) was obsd. for hydrophobic neutral DOM fractions, followed by lower ΦT,n values for hydrophobic acid, base, and hydrophilic acid DOM fractions, resp. An extd. wastewater biomass DOM sample contained arom. protein- and humic-like material and was characteristic of bacterial sol. microbial products. Arom. carbon and the presence of specific arom. compds. (as indicated by solid-state 13C NMR and FTIR data) resulted in EEMs that aided in differentiating wastewater effluent DOM from drinking water DOM.
- 21Prest, E. I.; Hammes, F.; van Loosdrecht, M. C. M.; Vrouwenvelder, J. S. Biological Stability of Drinking Water: Controlling Factors, Methods, and Challenges. Front. Microbiol. 2016, 7 (45), 1– 24, DOI: 10.3389/fmicb.2016.00045Google ScholarThere is no corresponding record for this reference.
- 22Ou, F.; McGoverin, C.; Swift, S.; Vanholsbeeck, F. Absolute bacterial cell enumeration using flow cytometry. J. Appl. Microbiol. 2017, 123 (2), 464– 477, DOI: 10.1111/jam.13508Google Scholar22https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2sXhtF2it73L&md5=0a6049fd8837aaa10684393c97df2e2aAbsolute bacterial cell enumeration using flow cytometryOu, F.; McGoverin, C.; Swift, S.; Vanholsbeeck, F.Journal of Applied Microbiology (2017), 123 (2), 464-477CODEN: JAMIFK; ISSN:1364-5072. (Wiley-Blackwell)Aim : To evaluate a flow cytometry protocol that uses ref. beads for the enumeration of live and dead bacteria present in a mixt. Methods and Results : Mixts. of live and dead Escherichia coli with live:dead concn. ratios varying from 0 to 100% were prepd. These samples were stained using SYTO 9 and propidium iodide and 6-μm ref. beads were added. Bacteria present in live samples were enumerated by agar plate counting. Bacteria present in dead samples were enumerated by agar plate counting before treatment with isopropanol. There is a linear relationship between the presented flow cytometry method and agar plate counts for live (R2 = 0·99) and dead E. coli (R2 = 0·93) concns. of c. 104 to 108 bacteria per mL within mixts. of live and dead bacteria. Conclusions : Reliable enumeration of live E. coli within a mixt. of both live and dead was possible for concn. ratios of above 2·5% live and for the enumeration of dead E. coli the lower limit was c. 20% dead. Significance and Impact of the Study : The ability to obtain abs. cell concns. is only available for selected flow cytometers, this study describes a method for accurate enumeration that is applicable to basic flow cytometers without specialized counting features. By demonstrating the application of the method to count E. coli, we raised points of consideration for using this FCM counting method and aim to lay the foundation for future work that uses similar methods for different bacterial strains.
- 23Fujioka, T.; Oshima, N.; Suzuki, R.; Khan, S. J.; Roux, A.; Poussade, Y.; Drewes, J. E.; Nghiem, L. D. Rejection of small and uncharged chemicals of emerging concern by reverse osmosis membranes: The role of free volume space within the active skin layer. Sep. Purif. Technol. 2013, 116, 426– 432, DOI: 10.1016/j.seppur.2013.06.015Google Scholar23https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3sXhtFOgtLfJ&md5=d387f3e43710678f5926dbb7d35c7a04Rejection of small and uncharged chemicals of emerging concern by reverse osmosis membranes: The role of free volume space within the active skin layerFujioka, Takahiro; Oshima, Nagayasu; Suzuki, Ryoichi; Khan, Stuart J.; Roux, Annalie; Poussade, Yvan; Drewes, Jorg E.; Nghiem, Long D.Separation and Purification Technology (2013), 116 (), 426-432CODEN: SPUTFP; ISSN:1383-5866. (Elsevier B.V.)Free-vol. hole-radii of the active skin layer of one seawater and 2 low pressure reverse osmosis (RO) membranes, namely SWC5, ESPAB, and ESPA2, resp., were evaluated using positron annihilation lifetime spectroscopy (PALS) with a slow positron beam. The results were related to the rejection of boric acid and eight N-nitrosamines to provide insights to the transport of these small solutes through RO membranes. At pH 8 (which is the exptl. pH in this study), these solutes are uncharged. PALS anal. showed that the SWC5 has the smallest mean free-vol. hole-radius (0.259 nm) among the three RO membranes studied. Correspondingly, the SWC5 membrane exhibited the highest rejection of boric acid and all N-nitrosamines. Results reported here also showed that the rejection of these chems. increased in the order of increasing mol. vol. The difference in their rejection amongst the 3 RO membranes studied was most apparent for those (i.e., boric acid and N-nitrosodimethylamine (NDMA)) with a small mol. vol. The EPSA2 and ESPAB were detd. to have mean free-vol. hole-radius of 0.289 nm. However, the ESPAB membrane had lower water permeability and showed considerably higher rejection of boric acid and NDMA than the ESPA2 membrane. These results suggest that in addn. to the mean free-vol. hole-radius, other membrane parameters and properties such as the free-vol. hole-radius distribution and thickness of the active skin layer can also play a role in governing the rejection of small and uncharged solutes by RO membranes.
- 24Park, S.; Hu, J. Y. Assessment of the extent of bacterial growth in reverse osmosis system for improving drinking water quality. J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2010, 45 (8), 968– 977, DOI: 10.1080/10934521003772386Google ScholarThere is no corresponding record for this reference.
- 25Ishida, K. P.; Cooper, W. J. Analysis of parameters affecting process efficiency, energy consumption, and carbon footprint in water reuse; WateReuse Research Foundation: Alexandria, VA, 2015.Google ScholarThere is no corresponding record for this reference.
- 26Liikanen, R.; Miettinen, I.; Laukkanen, R. Selection of NF membrane to improve quality of chemically treated surface water. Water Res. 2003, 37 (4), 864– 872, DOI: 10.1016/S0043-1354(02)00412-8Google ScholarThere is no corresponding record for this reference.
- 27Laurent, P.; Servais, P.; Gatel, D.; Randon, G.; Bonne, P.; Cavard, J. Microbiological quality: Before and after nanofiltration. J. - Am. Water Works Assoc. 1999, 91 (10), 62– 72, DOI: 10.1002/j.1551-8833.1999.tb08716.xGoogle Scholar27https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADyaK1MXmslOrur4%253D&md5=b2aa68eb9a35ed9dee6bc8f496b2dadcMicrobiological quality before and after nanofiltrationLaurent, Patrick; Servais, Pierre; Gatel, Dominique; Randon, Guy; Bonne, Pascal; Cavard, JacquesJournal - American Water Works Association (1999), 91 (10), 62-72CODEN: JAWWA5; ISSN:0003-150X. (American Water Works Association)The authors investigated microbiol. behavior of a distribution system supplied initially with biol. treated water and then with nanofiltered water. Their purpose was to identify and evaluate the changes in microbiol. water quality attributable to modifications in water treatment at the plant. During the course of the study, all data from various indicators of microbiol. quality (i.e., heterotrophic plate counts, coliform enumeration, total direct counts, and fixed bacterial biomass) showed similar trends. Results indicated that the use of nanofiltration allows utilities to reduce chlorination of treated water and at least maintain or increase the microbiol. quality of distributed water for areas with high residence times.
- 28Pype, M.-L.; Lawrence, M. G.; Keller, J.; Gernjak, W. Reverse osmosis integrity monitoring in water reuse: The challenge to verify virus removal – A review. Water Res. 2016, 98, 384– 395, DOI: 10.1016/j.watres.2016.04.040Google Scholar28https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XnvFSjsbw%253D&md5=f397be33b159a97d02ccfce38be68652Reverse osmosis integrity monitoring in water reuse: The challenge to verify virus removal - A reviewPype, Marie-Laure; Lawrence, Michael G.; Keller, Jurg; Gernjak, WolfgangWater Research (2016), 98 (), 384-395CODEN: WATRAG; ISSN:0043-1354. (Elsevier Ltd.)A review with many refs. A reverse osmosis (RO) process is often included in the treatment train to produce high quality reuse water from treated effluent for potable purposes because of its high removal efficiency for salinity and many inorg. and org. contaminants, and importantly, it also provides an excellent barrier for pathogens. In order to ensure the continued protection of public health from pathogen contamination, monitoring RO process integrity is necessary. Due to their small sizes, viruses are the most difficult class of pathogens to be removed in phys. sepn. processes and therefore often considered the most challenging pathogen to monitor. To-date, there is a gap between the current log credit assigned to this process (detd. by integrity testing approved by regulators) and its actual log removal capability as proven in a variety of lab. and pilot studies. Hence, there is a challenge to establish a methodol. that more closely links to the theor. performance. In this review, after introducing the notion of risk management in water reuse, we provide an overview of existing and potentially new RO integrity monitoring techniques, highlight their strengths and drawbacks, and debate their applicability to full-scale treatment plants, which open to future research opportunities.
- 29Liu, G.; Lut, M. C.; Verberk, J. Q. J. C.; Van Dijk, J. C. A comparison of additional treatment processes to limit particle accumulation and microbial growth during drinking water distribution. Water Res. 2013, 47 (8), 2719– 2728, DOI: 10.1016/j.watres.2013.02.035Google ScholarThere is no corresponding record for this reference.
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