Are Indicator Microorganisms Predictive of Pathogens in Water?
Abstract
:1. Introduction
2. Origin of the Microbiological Contamination of DWSs and DW
3. Role of the IMs for the Evaluation of DW Safety
3.1. Total Coliforms
3.2. Thermotolerant Coliforms
3.3. Escherichia coli
3.4. Intestinal Enterococci
3.5. Heterotrophic Plate Count (HPC)
3.6. Clostridium perfringens and Its Spores
3.7. Bacteroides spp.
3.8. Coliphages
3.9. Methanobrevibacter smithii
3.10. Pepper Mild Mottle Virus
4. Analysis of the Relationship between IMs and Pathogens in DWSs and in DW
4.1. Groundwater
4.2. Surface Water
4.3. Rainwater
4.4. Drinking Water
5. Discussion
- The intrinsic characteristics of microorganisms, which, although similar, are not identical and therefore may present physiological differences, different decay rates, and different survival and multiplication capacities in the water environment [40];
- Seasonal variations, which affect the sources of water contamination and thus the presence and concentration of both IMs and pathogenic microorganisms (e.g., extreme weather events, urban discharges in tourist cities) [71];
- The high temporal and spatial fluctuation characterising pathogenic microorganisms, in contrast to IMs, in water environments, due to biotic and environmental factors, intrinsic characteristics of the pathogen, and its circulation in the population. This transient nature of pathogen occurrence in water means that correlation with IMs may exist at one point in time and not at another, even at the same geographic site [32]. In such a situation, the frequency of sampling becomes paramount to capture the moment of contamination [61];
- The fact that, especially in waters that are usually not heavily contaminated such as GW or DW, pathogens may not actually be present or may be present below the detection limit of the analytical method (e.g., human enteric viruses), which makes it difficult to assess the relationship with IMs [32];
- The number of samples on which the association is evaluated, as numerically large samples allow for smaller errors and thus greater reliability of the results of applied statistics. Several studies considered in this review have evaluated a small number of samples (n ≤ 22) [52,53,55,58,67]. The correlations found in these studies clearly have a different weight than those assessed on larger datasets (e.g., n = 1656 [50]; n = 964 [48]; n = 415 [69]), so it would be necessary to expand the sample size to validate the indicator–pathogen correlation;
- The volume of water sampled, as microorganisms in water environments are not uniformly distributed. This means that taking a few large-volume samples or many small-volume samples may lead to different results. Typically, the detection of pathogens requires large volumes of water (10–1000 L), because of their transient presence and generally lower concentrations than those of IMs. In contrast, the detection of IMs is normally carried out on 100–250 mL [66,74];
- The use of different detection methods (culture or molecular), characterised by different efficiency, sensitivity, and specificity, for the detection of IMs and pathogens may compromise correlation evaluation. Typically, indicator detection, especially of traditional indicators but not only, is based on the use of simple, rapid, and cost-effective culture techniques. Conversely, for most pathogens, the available culture techniques are expensive, difficult, time-consuming, and have low efficiency. For these reasons, pathogenic microorganisms are usually identified by molecular methods (PCR, qPCR, RT-qPCR). In several studies described in this work, a better ability of IMs to point out pathogen presence/absence was found when both targets were searched using the same detection method (i.e., molecular method) [59,60,62,65].
6. DW Guidelines and Quality Standards
6.1. WHO Guidelines
6.2. US EPA Regulations
- Maximum Contaminant Level Goal (MCLG) is the level of a contaminant in DW below which there is no known or expected health risk (also including risk for most sensitive people, such as infants, children, pregnant women, the elderly, and immunocompromised individuals). This goal allows for a margin of safety and is non-enforceable;
- Maximum Contaminant Level (MCL) is the highest level of a contaminant that is allowed in DW. MCLs are set as close as possible to MCLGs using the best available treatment technology and considering costs. These are enforceable standards;
- Treatment Technique (TT) is a required process intended to reduce the level of a contaminant in DW.
6.3. Canadian Guidelines
6.4. Australian Guidelines
6.5. Directive (EU) 2020/2184
7. A Focus on Quantitative Microbial Risk Assessment (QMRA)
8. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
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IM | Significance | Surrogate for Pathogens |
---|---|---|
Total coliforms | Process indicators | - |
Thermotolerant coliforms | Indicators of faecal contamination by humans and warm-blooded animals | - |
Escherichia coli | Indicator of faecal contamination by humans and warm-blooded animals | Surrogate for bacterial enteric pathogens: pathogenic E. coli, Salmonella, Shigella |
Intestinal enterococci | Indicators of faecal contamination by humans and warm-blooded animals | - |
Heterotrophic plate count (HPC) | Process and water quality indicator | - |
Clostridium perfringens and its spores | Indicator of remote faecal contamination by humans and warm-blooded animals | Surrogate for protozoan pathogens: Cryptosporidium, Giardia |
Bacteroides spp. | Indicators of faecal contamination by humans and warm-blooded animals, they can be used to identify the source of faecal pollution | - |
Coliphages | Indicators of faecal contamination by humans and warm-blooded animals | Surrogate for enteric viruses |
Methanobrevibacter smithii | Indicator of human faecal contamination | - |
Pepper mild mottle virus (PMMoV) | Indicator of human faecal contamination | Possible surrogate for enteric viruses |
Reference and Publication Year | Country | GW Type | Number of Samples | IMs and Detection Method | Pathogens and Detection Method | Correlation |
---|---|---|---|---|---|---|
[48], 2020 | Minnesota, USA | Disinfected and undisinfected GW from public water supply wells 1 | 964 | Culture method: total coliforms, E. coli Molecular method: PMMoV, human Bacteroides HF183, Bacteroidales-like HumM2 | Molecular method: C. jejuni, enteropathogenic E. coli, Shiga-toxin-1- and 2-producing bacteria, Salmonella, adenovirus, human enterovirus, human polyomavirus, norovirus GI and GII, rotavirus group A, hepatitis A virus, Giardia, Cryptosporidium | E. coli (detected in only 3 samples) not considered for correlation. Hepatitis A virus, norovirus GI, enteropathogenic E. coli, and Shiga-toxin-1-producing bacteria never detected. Positive significant: for all IMs except PMMoV on total samples (logistic regression, p < 0.01). Not significant: for any IMs at each well (p > 0.05). |
[49], 2018 | Montana, USA | GW used as DW | 57 2 | Culture method: total coliforms, E. coli, HPC | Culture method: Mycobacterium, Helicobacter Molecular method: Mycobacterium, Helicobacter | Positive significant: between HPC and Mycobacterium (logistic regression, p = 0.05). |
[50], 2016 | Apulia region, Italy | GW from wells for emergency use | 1656 | Culture method: E. coli, total coliforms, enterococci, HPC 22 °C and 37 °C | Culture method: Salmonella spp. | Positive significant: between Salmonella spp. and E. coli, total coliforms and enterococci (Spearman correlation coefficient, p < 0.0001). No indication on correlation for HPC. |
[51], 2012 | Bangladesh | GW from shallow tube wells as a primary source of DW | 50 | Culture method: total coliforms, E. coli, F+ RNA coliphages Molecular method: E. coli | Molecular method: Shigella, Vibrio, pathogenic E. coli, rotavirus | Positive significant: between pathogenic E. coli and culturable E. coli, total coliforms and F+ RNA coliphages; between molecular E. coli and Shigella (Spearman rank correlations, p < 0.05). |
[52], 2011 | Katmandu Valley, Nepal | GW from shallow wells for daily water supply | 9 | Culture method: E. coli, total coliforms Molecular method: F-RNA coliphages | Immunofluorescent microscopy: Cryptosporidium, Giardia Molecular method: human adenoviruses, noroviruses GI and GII | Positive significant: 3 samples negative for E. coli and target pathogens; 5/6 E. coli-positive samples also positive for at least one of target pathogens (chi-square test, p < 0.05). No indication on correlation of pathogens with total coliforms and F-RNA coliphages. |
[53], 2001 | Pennsylvania, USA | Private untreated well water consumed as DW | 22 | Culture method: E. coli | Culture method: H. pylori | Positive significant: between E. coli and H. pylori (Fisher’s exact test, p = 0.0011). |
Reference and Publication Year | Country | SW Type | Number of Samples | Indicators and Detection Method | Pathogens and Detection Method | Correlation |
---|---|---|---|---|---|---|
[55], 2021 | North Carolina, USA | River water and sewage-impacted reservoirs, both sources for DW treatment plants | 22 | Culture method: total coliforms, E. coli, Enterococcus spp., C. perfringens, somatic and F+ coliphages | Immunofluorescent microscopy: Cryptosporidium, Giardia Culture method: Salmonella spp. Molecular method: adenovirus, norovirus | Positive significant:
Not significant: for any IMs by treatment plant (n = 5) (Spearman’s rank correlation, p > 0.05). Norovirus never detected. |
[56], 2019 | China | Tiaoxi River, an important source of water supply | 45 | Culture method: faecal coliforms Molecular method: Bacteroidales (total, human-, swine-, and avian-associated) | Molecular method: C. jejuni, pathogenic Leptospira spp., Shigella spp., Shiga-toxin-producing E. coli (STEC), E. coli O157:H7 | Positive significant: between STEC and total and human Bacteroidales (Spearman’s coefficient correlation, p < 0.05). |
[57], 2019 | Bogotá, Colombia | Catchment of raw superficial waters | 155 | Culture method: total coliforms, E. coli, spores of sulphite-reducing clostridia | Molecular method: H. pylori | Not significant: for any IMs (Spearman correlation coefficient and Tau-b Kendall correlation coefficient, p > 0.05). |
[58], 2018 | Nepal | Bagmati River water used untreated for domestic use | 18 | Culture method: total coliforms, E. coli Molecular method: E. coli, Enterococcus spp., human Bacteroidales HF183, PMMoV | Immunofluorescent microscopy: Cryptosporidium, Giardia Molecular method: Aichi virus 1, enteroviruses, human cosaviruses, human adenoviruses, noroviruses GI and GII, group A rotaviruses, saliviruses | Positive significant: between all IMs and total human enteric viruses (bivariate correlation with Pearson coefficients, p < 0.05) |
[59], 2015 | Singapore | Tributaries and reservoir used for DW | 148 | Culture method: E. coli, enterococci, somatic and F-coliphages Molecular method: E. coli, enterococci, Bacteroides thetaiotaomicron, M. smithii | Culture method: Salmonella spp. Molecular method: rotavirus, astrovirus, norovirus GI and GII, adenovirus | Positive significant: between Salmonella spp. and E. coli, enterococci, somatic and F-coliphages, and B. thetaiotaomicron (Spearman’s rank correlation, p < 0.05); between adenovirus and norovirus GII and molecular E. coli (p < 0.05) and molecular enterococci (p < 0.01); between norovirus GII and M. smithii (p < 0.05) and B. thetaiotaomicron (p < 0.01); between norovirus GI and M. smithii (p < 0.01). |
[60], 2015 | Singapore | Marina Reservoir, an important source of DW | 75 | Culture method: somatic and F-coliphages Molecular method: F-coliphages | Molecular method: adenovirus, norovirus GI and GII, astrovirus, rotavirus | Positive significant: between cultural F-coliphages and norovirus GII and rotavirus; between molecular human-specific GII coliphages and all human enteric viruses (Kendall Tau-b correlation, p < 0.05). |
[61], 2014 | Luxembourg | Raw SW (sub-catchments, river, reservoir, and inlet of a DW treatment plant) | 121 | Culture method: E. coli | Immunofluorescent microscopy: Cryptosporidium, Giardia | Positive significant: between E. coli and Giardia in the river and both protozoa in the reservoir and at the inlet of the DW treatment plant (nonparametric Spearman rank correlation test, p < 0.05). |
[62], 2014 | Singapore | Reservoir for water supply | 65 | Culture method: somatic and male-specific coliphages | Molecular method: adenovirus, norovirus GI and GII, astrovirus, rotavirus | Positive significant: between male-specific coliphages and norovirus GI and GII (Kendall’s Tau-b correlation, p < 0.05). |
[63], 2013 | Canada | Raw lake water entering three DW treatment plants (DWTP1, DWTP2, DWTP3) | 298 | Culture method: total coliforms, E. coli, enterococci, clostridia Molecular method: human Bacteroidales HF183 | Culture method: thermophilic Campylobacter, cultivable enteric viruses Immunofluorescent microscopy: Cryptosporidium, Giardia Molecular method: Cryptosporidium, Giardia | Positive significant: between enterococci and enteric viruses in DWTP1 and DWTP3 influents (Spearman rank correlation test, p < 0.05); between clostridia and enteric viruses in DWTP1 (p < 0.05); between clostridia and Cryptosporidium in DWTP2 influent (p < 0.05). |
[64], 2010 | North Carolina, USA | Creek and pond tributaries of Jordan Lake, a DWS | 83 | Culture method: faecal coliforms, E. coli, enterococci, C. perfringens spores, somatic and male-specific coliphages | Culture method: Salmonella spp. | Positive significant: between Salmonella spp. and faecal coliforms, E. coli, enterococci, C. perfringens spores, and somatic coliphages (Spearman rank correlation, p < 0.05). |
[65], 2010 | Netherlands | Source water for DW production (intake area or upstream of a source water intake area) | 75 | Culture method: somatic and F-specific coliphages | Culture method: enteroviruses, reoviruses Molecular method: noroviruses, rotaviruses | Positive significant: between the two coliphages and enteroviruses (p < 0.0005). |
[66], 2010 | Utah, USA | Raw SW of seven DW treatment plants (reservoir and stream) | 228 | Culture method: E. coli | Immunofluorescent microscopy: Cryptosporidium | Negative significant: between E. coli and Cryptosporidium in winter for reservoir samples (nonparametric Spearman correlations). |
[67], 2008 | New York, USA | Tributaries of the Kensico Reservoir, a primary source of DW for the city of New York | 16 | Culture method: faecal coliforms, E. coli, enterococci, C. perfringens spores, somatic and F+ coliphages | Immunofluorescent microscopy: Cryptosporidium, Giardia | Not significant: for any IMs (nonparametric Spearman rank statistical test, p > 0.5). |
[68], 2004 | São Paulo, Brazil | SW used to supply DW | 278 | Culture method: faecal coliforms, C. perfringens | Immunofluorescent microscopy: Giardia, Cryptosporidium | Positive significant: between IMs and Giardia for total samples (Spearman rank correlation coefficient, p < 0.0001) and for only 3/10 watersheds (p < 0.05). Cryptosporidium not considered for correlation (low number of positive samples). |
[69], 2000 | Canada | Raw river water | 415 | Culture method: total coliforms, faecal coliforms, C. perfringens | Culture method: cultivable human enteric viruses Immunofluorescent microscopy: Cryptosporidium, Giardia | Positive significant: between all IMs and all pathogens (Spearman correlation analysis, p < 0.001; logistic regression analysis, p ≤ 0.001). |
Reference and Publication Year | Country | RW Type | Number of Samples | Indicators and Detection Method | Pathogens and Detection Method | Correlation |
---|---|---|---|---|---|---|
[70], 2018 | Australia | Roof-harvested RW for potable and non-potable use | 144 | Culture method: E. coli, Enterococcus spp. Molecular method: E. coli, Enterococcus spp. | Molecular method: enteropathogenic E. coli, Shiga-toxin-producing E. coli, Shigella spp., Salmonella spp., C. jejuni, C. lari, C. perfringens, Listeria monocytogenes, V. cholera, V. parahaemolyticus | Only Shigella spp. was detected. Negative significant: between IMs and Shigella spp. (odds ratio, p < 0.05). |
[71], 2017 | Australia | Roof-harvested RW for potable and non-potable use | 144 | Culture method: E. coli, Enterococcus spp. | Molecular method: M. avium, M. intracellulare | Not significant: for any IMs (nonparametric Kendall’s Tau correlation, p > 0.05). |
[72], 2016 | Australia | Roof-harvested RW for potable and non-potable use | 134 | Culture method: total coliforms, E. coli, Enterococcus spp. | Molecular method: M. avium, M. intracellulare | Positive significant: between M. intracellulare and E. coli and total coliforms (nonparametric Kendall’s Tau correlation, p < 0.05). Negative significant: between Enterococcus spp. and M. avium (p < 0.05). |
[73], 2014 | Australia | Roof-captured RW for potable and non-potable use | 72 | Culture method: E. coli, Enterococcus spp. | Molecular method: A. hydrophila | Not significant: for any IMs (binary logistic regression analysis, p > 0.05). |
[74], 2010 | Australia | Roof-harvested RW for drinking and non-potable use | 100 | Culture method: E. coli, enterococci, spore-forming C. perfringens | Molecular method: A. hydrophila, C. coli, C. jejuni, Salmonella, E. coli O157, Giardia lamblia, Cryptosporidium parvum | Not significant: for any IMs (binary logistic regression, p > 0.05). E. coli O157 and C. parvum never detected. |
[75], 2001 | Auckland, New Zealand | Domestic roof-collected RW consumed as DW | 125 | Culture method: HPC, total coliforms, faecal coliforms, enterococci | Culture method: Salmonella spp., Campylobacter spp., Aeromonas spp. Immunofluorescent microscopy: Cryptosporidium, Giardia | Positive significant: between Aeromonas spp. and all IMs (p < 0.05). Campylobacter spp. and Giardia never detected. |
Ever-Present Correlation | |
---|---|
IM | Pathogen |
E. coli | Adenovirus Norovirus Shigella spp. |
Bacteroides | Norovirus Salmonella spp. Shiga-toxin-2-producing bacteria (including E. coli) |
Ever-Absent Correlation | |
IM | Pathogen |
E. coli | Campylobacter (coli and jejuni) Rotavirus |
Enterococci | Campylobacter (coli and jejuni) Cryptosporidium Giardia |
C. perfringens and its spores | Campylobacter (coli and jejuni) Helicobacter |
PMMoV | Cryptosporidium Giardia |
IM | Pathogen |
---|---|
Total coliforms | Cryptosporidium Salmonella spp. |
E. coli | Giardia Salmonella spp. |
Enterococci | Salmonella spp. |
WHO Guidelines | US EPA Regulations | Canadian Guidelines | Australian Guidelines | Directive (EU) 2020/2184 | ||||
---|---|---|---|---|---|---|---|---|
Guideline values | MCLG 2 | MCL 2 | TT 2 | Maximum acceptable concentration | Treatment target | Non-mandatory standards | Parametric values | |
Total coliforms | Zero | 5.0% 3 | - | 0/100 mL 7 | - | 0/100 mL 8 | ||
Thermotolerant (faecal) coliforms | 0/100 mL | Zero | - 4 | - | 0/100 mL | |||
E. coli | 0/100 mL 1 | Zero | - 4 | - | 0/100 mL | - | 0/100 mL | 0/100 mL 8 |
Intestinal enterococci | 0/100 mL 8 | |||||||
HPC | N/A | <500 colonies per millilitre | (HPC 22 °C) No abnormal change | |||||
C. perfringens including spores | 0/100 mL 9 | |||||||
Coliphages | 0/100 mL | (Somatic coliphages) 50 PFU/100 mL (for raw water) 10 | ||||||
Cryptosporidium | Zero | - | 99% removal 5 | - | Minimum 3 log removal and/or inactivation of cysts and oocysts | |||
Giardia lamblia | Zero | - | 99.9% removal or inactivation | - | Minimum 3 log removal and/or inactivation of cysts and oocysts | |||
Legionella | Zero | - | - 6 | <1000 CFU/L 11 | ||||
Enteric viruses | Zero | - | 99.9% removal or inactivation | - | Minimum 4 log reduction (removal and/or inactivation) |
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Richiardi, L.; Pignata, C.; Fea, E.; Bonetta, S.; Carraro, E. Are Indicator Microorganisms Predictive of Pathogens in Water? Water 2023, 15, 2964. https://doi.org/10.3390/w15162964
Richiardi L, Pignata C, Fea E, Bonetta S, Carraro E. Are Indicator Microorganisms Predictive of Pathogens in Water? Water. 2023; 15(16):2964. https://doi.org/10.3390/w15162964
Chicago/Turabian StyleRichiardi, Lisa, Cristina Pignata, Elisabetta Fea, Silvia Bonetta, and Elisabetta Carraro. 2023. "Are Indicator Microorganisms Predictive of Pathogens in Water?" Water 15, no. 16: 2964. https://doi.org/10.3390/w15162964