Article pubs.acs.org/est
Adapting Enzyme-Based Microbial Water Quality Analysis to Remote Areas in Low-Income Countries Adam Abramson,* Maya Benami, and Noam Weisbrod Department of Environmental Hydrology & Microbiology, Zuckerberg Institute for Water Research, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben-Gurion, 84990 Israel S Supporting Information *
ABSTRACT: Enzyme−substrate microbial water tests, originally developed for efficiency gains in laboratory settings, are potentially useful for on-site analysis in remote settings. This is especially relevant in developing countries where water quality is a pressing concern and qualified laboratories are rare. We investigated one such method, Colisure, first for sensitivity to incubation temperatures in order to explore alternative incubation techniques appropriate for remote areas, and then in a remote community of Zambia for detection of total coliforms and Escherichia coli in drinking-water samples. We sampled and analyzed 352 water samples from source, transport containers and point-of-use from 164 random households. Both internal validity (96−100%) and laboratory trials (zero false negatives or positives at incubation between 30 and 40 °C) established reliability under field conditions. We therefore recommend the use of this and other enzyme-based methods for remote applications. We also found that most water samples from wells accessing groundwater were free of E. coli whereas most samples from surface sources were fecally contaminated. We further found very low awareness among the population of the high levels of recontamination in household storage containers, suggesting the need for monitoring and treatment beyond the water source itself.
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INTRODUCTION Routine monitoring of microbial water quality is one of the most effective means of quantifying, and thereby reducing, risks to public health in remote areas of low-income countries. The disease burden, measured in disability-adjusted life years, associated with diarrhea from consuming contaminated drinking water is over 30 times greater in low- vs high-income regions.1 These areas are also the most difficult and costly to monitor. Standard laboratory-based microbial water tests, including multiple-tube fermentation, membrane-filter technique,2 and polymerase chain reaction (PCR),3 have certain technical requirements that make them particularly unsuitable for analyzing water samples from rural areas in developing countries. Each of these techniques requires (1) expensive equipment; (2) careful use of aseptic technique during collection, analysis and storage; (3) highly trained personnel; (4) a temperature-controlled incubator; and (5) a 24 h time constraint for analysis initiation.4 Distance and low levels of infrastructure greatly inhibit the feasibility of conducting these standard procedures in off-site laboratories, both technically and due to increased costs. As a result, a trade-off has traditionally existed between the remoteness of a monitoring effort and cost-effectiveness.5−7 As costs of off-site analytical techniques increase with remoteness, technical feasibility may reach a threshold. At a certain point, conventional laboratories become useless as remoteness pushes water sampling and transport time beyond © 2013 American Chemical Society
the 24 h limit. Coincidentally, remote water-testing efforts are limited in scope and depth. Comprehensive routine monitoring is, in practice, practically nonexistent in low-income countries. Along with the approaching culmination of the Millennium Development Goals is the emerging acknowledgment that efforts must be expanded beyond the development of improved sources to include monitoring of drinking water quality both at the source and point-of-use (POU).8,9 As Bain et al.10 demonstrate, there are 44 microbial water tests currently available for meeting compliance, surveillance, operational, or other monitoring objectives in low- or mediumresource contexts. In this study, we focus on the need to conduct compliance monitoring for ensuring that samples meet regulatory standards. In this case, it is important for a test to be able to detect contamination corresponding to the WHO’s threshold of 1 CFU E. coli per 100 mL. In addition, regulatory approval of the methodology is necessary, such as by the U.S. EPA or through inclusion in the Standard Methods for the Examination of Water and Wastewater.4 When these requirements are considered along with the technical challenges associated with remote areas, only 6 of the 44 methodologies are found feasible for conducting compliance testing in remote Received: Revised: Accepted: Published: 10494
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based methods in Supporting Information S1. Thus, four tests may be considered potentially appropriate: Colisure, Colilert, Colilert-18, and Colitag. These tests all share the following characteristics: (1) they are chromogenic and fluorogenic presence−absence (P-A) enzyme−substrate tests for fecal and total coliforms; (2) they test standard, 100 mL samples; (3) they consist of only a sampling container and a powdered agar, and require incubation and a hand-held UV light; (4) the cost of consumables is between $4.50 and $5.00 per test; and (5) they are approved for incubation at 35 ± 0.5 °C.10,25−27 These tests differ only in the specific enzymes and substrates used (to metabolize coliforms, Colilert uses ONPG and MUG, Colisure uses CPRG and MUG, and Colitag uses ONPG and MUG along with a buffer medium, TMAO), storage temperature and shelf life, and the duration of the test. Of these techniques, Colisure (IDEXX Technologies, Westbrook, ME) was used in this study because it is highly cited in the literature. Most of these citations are for testing drinking water samples with low levels of contamination. In these cases, its accuracy has been previously documented,28,29 and it has been shown to be superior to certain accepted reference methods in the detection of chlorine-injured coliforms and E. coli under conditions that resemble those of contaminated drinking water.30,31 Colisure (and other enzymebased approaches) is also emerging as an important tool for testing environmental water samples.32−35 For example, it is the most common approach for testing recreational waters in the Great Lakes region of the US.32 The test has been shown to possess acceptable ability to suppress non-coliform bacteria,24 although false readings are more common in environmental samples. This is true for both enzyme-based as well as some standard methodologies; Wohlsen, et al. reported a coefficient of variation of 38% for Colisure, and 44.8% with membrane filtration when testing environmental samples.36 This suggests that its accuracy when testing environmental samples may be compromised, but no more than that of conventional methods.
areasall of which are enzyme-based: Colisure, Colilert, Colilert-18, Colitag, E*Colite, and Readycult. Enzyme-based methodologies, accepted as the industry standard for microbiological water testing in laboratories, possess untapped potential for use as microbial field tests for low-cost, rapid assessments of water quality in remote areas.11 Unlike other field tests, they are inexpensive and simple to implement. Through simultaneous chemical targeting of coliform-specific enzymatic processes with inhibition of noncoliform species, the entire process can be conducted in a single sterile container, internalizing the aseptic environment while simultaneously allowing for the simple analysis of an entire 100 mL sample. Neither dilution nor filtration, and only simple aseptic procedureswearing latex gloves and ensuring proper sampling technique, are required. Nevertheless, the recent emergence of such methods, primarily for the benefit of in-lab convenience and gains in time efficiency, has largely overlooked the rural water sector, where public health gains from reliable water-quality data are high. Most studies investigating enzyme-based methods have focused on the advantages of Colisure or its sister technique, Colilert, in detecting or enumerating E. coli in microbial laboratories.12−18 However, their application for remote on-site monitoring in developing countries has been overlooked: to our knowledge, only three studies have applied these advantages to water sampling in developing countries,19,20 and only one of those conducted a remote on-site analysis.21 No studies to date have investigated enzyme-based methodologies for on-site compliance testing relative to the World Health Organization (WHO) guideline for drinking water.1 While enzyme−substrate tests remove most obstacles, the challenge of achieving and maintaining standardized incubation regimes remains a central obstacle to expanding water testing into low resource settings. Bain et al., for example, deem these six approaches ‘not ideal’ for analysis without a basic laboratory or clean space with electricity, presumably due to this need for lab-grade incubation procedures.10 Attempts have been made to overcome this by alternative incubation mechanisms. The Aquatest, a recently developed Most Probable Number test, uses boiled water to maintain incubation temperatures.10 Chuang et al. investigated the EC-Kita combination of Colilert and Petrifilmusing a waistbelt incubator operating on body heat alone.21,22 Brown et al. explored the feasibility of ambient temperature incubation in tropical areas with three microbial tests, including Colilert, and found that test accuracy was only marginally compromised.23 These studies provide evidence that the incubation temperature ranges may be expanded without sacrificing the accuracy of enzyme-based methods. The purpose of this study was to (1) test the accuracy of one enzyme-based method under a wider range of incubation temperatures than currently approved; (2) develop a simple, low-cost incubator for field use; (3) assess the technical feasibility of this adapted approach in a remote community for compliance testing relative to the WHO guideline for drinking water; (4) use this method to trace the fecal-contamination pathway and its relationship to user perceptions of water quality; and (5) compare the cost-effectiveness of this method to other feasible options for remote analysis. Of the six enzyme-based methods mentioned above, two (Readycult and E*Colite) were demonstrated to perform insufficiently in laboratory tests conducted by Olstadt et al.24 We present further details of a comparative analysis of enzyme-
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EXPERIMENTAL SECTION Temperature and Incubator Testing. The sampling and analytical procedures for Colisure are simple (see Supporting Information S2). To find an appropriate solution for the incubation challenges mentioned above, we conducted a preliminary investigation of the method’s sensitivity to temperature. This was conducted in a microbial laboratory by testing triplicate samples of sterile bottles with 100 mL sterile water inoculated with a 1 μL loop from frozen cultures of Staphylococcus aureus (ATCC 49834), Enterococcus faecalis (ATCC 10100), Klebsiella pneumonia (ATCC 10031), or Escherichia coli (MG 1655). A fourth triplicate of 100 mL of raw toilet water was tested in order to investigate the methodology with water resembling samples encountered in the field. Although exact contamination levels were not determined, the inoculation ensured that at least one viable cell was present in each sample while allowing for a degree of variation common in environmental water samples. These were incubated in a scientific-grade incubator in the laboratory at 25, 27, 30, 35, 37, 40, and 42 °C. In order to demonstrate the feasibility of other incubation techniques, a low-cost alternative was constructed from a small, temperature-sensitive space heater and a large cardboard box with insulating blankets. At the study site, this incubator was calibrated with a CR10X data logger (Campbell Scientific, Logan, UT) recording in situ water-sample temperatures by 10495
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an additional sampling point was added to the second (rainy season) survey: the household’s drinking cup.
placing three thermocouples in different Colisure watersampling bottles located at different distances from the heat source to determine the temperature range during incubation. The incubator was also used to incubate the samples. The main advantage of this device is that it is lightweight (consisting only of a blanket, cardboard box, and small space heater) and inexpensive. Study Site. The field study was performed in Simango Ward, a rural municipal subdistrict consisting of 15 villages in the Kazungula District of Southern Province, Zambia. It is located 57 km north of Livingstone municipal center. Mean village size is 51.7 households, and for an estimated ward size of 300 km2, population density is roughly two households or 13 people per km2. Recent surveys indicate that 77.2% of the households in this catchment use improved water services (in this case, boreholes with hand pumps), mean water-fetching time is 30.4 ± 1.29 min, and per capita water use averages 57.8 ± 5.3 L per day.37 Average yearly precipitation in the region is 650 mm, 90% of it falling between December and February.38 Most of the residents conduct rain-fed farming of maize, which is the staple food, and supplement their subsistence with low levels of cash income: average income levels of $0.22 ± 0.078 per capita per day are well below the global poverty line of $1.25 per capita per day.37 Survey Instrument. Two sampling efforts were conducted: one during the dry season (July 2011) in which 171 water samples38 sources and 133 containerswere taken from 101 households, and one during the rainy season (February 2012) in which 181 water samples37 sources, 80 containers, and 64 drinking cupswere taken from 63 households. These 164 households were randomly visited by a paired team of visiting and local Tonga-speaking surveyors who administered two separate sections of the survey instrument. The first section included household questions related to water use, sanitation, and water-quality perceptions. User perceptions of water quality for source, transport, and storage points were rated according to four statements ranging from “I fear very much that someone may get sick f rom it” to “I am sure that no one will get sick f rom it.” The second section was a mixed-methods observation activity consisting of photographs of storage and transport (if different from storage) containers, written notes of respondent behavior, and testing household water samples using the Colisure kit. Water samples were taken by visiting students using latex gloves and, if it was not possible to pour the water sample directly into the Colisure container, a sterile 50 mL container was used to draw water from the source. For point-ofuse (POU) drinking samples, heads of household were asked to pour water into the sample cup for testing in the same way they would pour water into their own cup, to ensure fidelity to regular water-drawing practices. Similarly, hand-washing practices were observed when the respondent complied. Samples were stored in a cooler for not more than 5 h before the sampling teams returned to the village center, where Colisure reagent agar was added and samples were placed in the field incubator. At the end of the visit, surveyors asked to see the household water source, which was sampled and photographed. If the household used different containers to transport and store the water, a sample was taken from the transport container after carrying water in it for several minutes. Thus, a total of two or three water samples were associated with each household interview. After review of the data from the first sampling event,
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RESULTS AND DISCUSSION Laboratory Testing of Colisure. As expected, samples spiked with E. faecalis and S. aureus did not change color or fluoresce under any of the incubation-temperature conditions. K. pneumonia, representing total coliform bacteria, was detected, as expected, at incubation temperatures between 25 and 37 °C, but not at 40 °C. E. coli was detected at all temperatures between 27 and 40 °C. Fecal contamination in toilet water was detected between 30 and 40 °C. Thus, recovery of E. coli was possible at incubation temperatures ranging from 30 to 40 °C with the Colisure method. The results are compiled in Table S3. These results suggest that the accuracy of this method may not be as dependent on precise incubation temperature regimes as standard protocol requires. If this is the case, alternative incubation techniques appropriate for lowresource areas may be used. Our findings concur with those of Brown et al., who found that analysis of samples using Colilert may be achieved with low levels of false negatives (4%) and false positives (3%) when incubated at ambient temperatures (i.e., without an incubator).23 It is especially remarkable that the ambient temperatures in their study were all below 30 °C. These findings demonstrate the need for a more robust study of the impact of incubation temperature on test accuracy to definitively determine acceptable temperature ranges of appropriate methods. Incubator Performance. Results of the makeshift field incubator demonstrated that its operating temperature range is within the range of reliability for incubation of total coliforms and E. coli. The in situ temperature range of means from 10 min intervals was between 28.85 and 42.4 °C, with a 7-day average temperature of 35.4 ± 1.3 °C. A detailed schematic is presented in Figure S1 and discussed in SI section S3. This suggested that a simple, low-cost, and readily available incubation device can be used in a makeshift manner for rural applications of Colisure microbial analysis. This particular device produced an incubation regime within accepted temperature specifications as the manufacturer recommends for some countries of 36 ± 2 °C.25 The only requirement for its implementation is a reliable source of electricity. There are certainly other possible techniques that would provide a temperature regime within the 30−40 °C range. Fire-heated rocks placed in an insulated box, for example, would remove the requirement for electricity. Preliminary trials using this method produced the same results as samples under standard incubation, although a more appropriately designed experiment would need to be performed for confirmation. The possibility of incubation at ambient temperature in tropical climates should also be considered. Internal Validity of Water Samples. A total of 352 water samples were taken from 164 households and analyzed with Colisure. Figure 1 presents the consistency of results from sources downstream of positive results. The small discrepancy in the E. coli results, mostly located among transport containers, may be partly due to respondent error, in which transport and storage water samples were stated to have been drawn from the same source, when in fact they were not. This is especially plausible for the 34% of households in the area regularly using multiple water sources.38 This suggests that a small fraction ( 1000), the method is not cost-effective compared to PFKs. This comparison assumes that there is no limit to the availability of trained external technicians or to the logistical resources necessary for implementing such approaches. As discussed above, logistical difficulties may reduce the feasibility of routine testing by outside experts in some remote areas, further enhancing the advantage of locally implemented approaches. The EC-Kit is comparable to Colisure at all sample sizes, and may be the most suitable approach in areas where surveillance, rather than compliance, testing is desired. Application of Findings. The tremendous logistical and economic challenges associated with monitoring water quality in remote populations of low-income countries require careful design of monitoring efforts. These results support previous findings that a significant disparity exists between the conformity of unimproved and improved water sources to microbial quality guidelinesmost improved sources are uncontaminated, and vice versa. With global water-development efforts recently reaching the MDGs for drinking water, most (86%) remote populations in low-income countries already have access to improved water sources.51 As such, monitoring efforts in most remote areas need not focus on ranking health risks associated with unimproved sourcesas promoted by the WHO’s ‘risk-level analysis’.1 Improved sources exist, and households should be using them. Instead, the highest priority for most remote areas lacking water-quality data is to monitor the long-term performance of improved water sources vis-a-vis their compliance to drinking water guidelines. For these sources, compliance testing could be implemented through either P-A or enumeration formats, as long as they possess the adequate sensitivity to detect 1 CFU E. coli per 100 mL. The second priority is to monitor the level of recontamination occurring from improved sources to the POU. Despite significant progress, water networks remain out of reach for a significant proportion of remote populations; only 46% in lowincome countries have access to household taps, while the rest carry water from either improved (40%) or unimproved (14%) water sources to their households.51 Tracing household-level recontamination is important for identifying countermeasures, such as POU treatment,42−45 which could be more effectively targeted where appropriate data are available. This study outlines the need for such tests to boost low community awareness of this recontamination. Again, compliance testing of POU water samples could be implemented through either P-A or enumeration formats. An important advantage of promoting these two applications is that the inaccuracy associated with testing heavily contaminated or environmental water samples would be minimized. As this study demonstrates, enzyme-based methods offer a promising, cost-effective alternative for achieving these two priority goals, especially where small sample sizes are needed. They are capable of obtaining microbial quality data for compliance testing using a simple, low-cost format that can be locally implemented. This may apply, for example, to local water service programs needing reliable measures of drinking water compliance. Likewise, nongovernmental organizations (NGOs), which are responsible for a high proportion of remote water improvements in low-income countries, often have small budgets, if any, for routine monitoring. As policy shifts continue toward community ownership of water services, local village
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ASSOCIATED CONTENT
* Supporting Information S
Enzyme-Based Approaches, Colisure Methodology, Field Incubator Performance, Water Sample Results by Containers, Regression Analysis, Comparative Analysis of Microbial Water Test Feasibility in Remote Areas, Cost Analysis of Microbial Tests. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*Tel.: +972 8 6563433; fax: +972 8 6596909. E-mail address:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors wish to thank the graduate students of the 2011 and 2012 Rural Water Development course as well as the Zuckerberg Institute for Water Research for making this study possible. We thank the Future Hope Church of Simango, Zambia, for the local help, and the Grace & Hope Charitable Trust, USA, for financial support.
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