Microb Ecol DOI 10.1007/s00248-015-0629-0
SHORT COMMENTARY
A Perspective on the Global Pandemic of Waterborne Disease Timothy E Ford 1 & Steve Hamner 2
Received: 13 January 2015 / Accepted: 14 May 2015 # Springer Science+Business Media New York 2015
Abstract Waterborne diseases continue to take a heavy toll on the global community, with developing nations, and particularly young children carrying most of the burden of morbidity and mortality. Starting with the historical context, this article explores some of the reasons why this burden continues today, despite our advances in public health over the past century or so. While molecular biology has revolutionized our abilities to define the ecosystems and etiologies of waterborne pathogens, control remains elusive. Lack of basic hygiene and sanitation, and failing infrastructure, remain two of the greatest challenges in the global fight against waterborne disease. Emerging risks continue to be the specter of multiple drug resistance and the ease with which determinants of virulence appear to be transmitted between strains of pathogens, both within and outside the human host. Keywords Hygiene . Sanitation . Infrastructure . Pathogens . Biofilms . Sequencing . E. coli
Introduction In order to present a perspective, it is important to look back through history to see how far we have come in the global fight against waterborne disease. I (Ford) am fortunate to be able to do that on a personal level, although my conclusion is that we have not come very far—at least in combatting diseases * Timothy E Ford [email protected] 1
School of Health Professions, Shenandoah University, Winchester, VA 22601, USA
2
Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
transmitted through contaminated drinking water in less developed countries. In his journals, my great ×4 grandfather wrote: BThe Cholera very much in progress – many victims here 30 or 40 in Jennings’ Buildings [a notorious slum off Kensington High Street, TF]. Salt particularly recommend to be used in small quantities for the cholera – a statement in the Spectator states this at full length & complains, justly, of the monopoly of the East India Company preventing the Natives enjoying this necessary healthy comfort & attributes the Cholera very much to this deprivation.^ Jonathan Bell, Kensington, London, January 1849. The Bstatement^ to which he refers is most likely Brown 1849 [1], which even today makes compelling reading. Although the mechanism discussed at the time was very different from the one we know today, oral rehydration therapy, at least the replenishment of salts is not completely an idea of the past 45 years or so [2]. What about the widely adopted low-cost water filtration systems that abound today? Again, I am informed by my predecessors, in this case my great ×2 grandfather, Reginald Craufuird Sterndale, who both wrote about and illustrated the basic process in 1881 [3]. At the time, he was Vice Chairman of the municipality of the suburbs of Calcutta and would later become Cantonment Magistrate, Dum Dum. To quote: BThere can be no doubt that, if the people could be induced to boil and filter the water used by them, that many dangerous waters might be thus used with comparative safety; but this cannot be expected, the very cost of fuel would prevent the poorer classes from taking this precaution; nor is it probably that they could, to any
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extent be brought to filter their drinking water, although materials for constructing a most efficient filter is to their hand, and at an outlay of but a few pice (former monetary unit) – a rough wooden stand, three ordinary porous earthenware culshis or jars, a small quantity of charcoal or sand being all that is necessary.^ Fig. 1. More than a century later, this situation remains unchanged for the world’s poorest citizens. During our 2004 study of water use patterns practiced by residents of Varanasi India, those interviewed reported using the heavily polluted Ganges River for everyday washing of dishes and laundry, personal hygiene, and as a primary source of drinking water [4]. The poorest among these residents devote their daily existence to procuring another day’s ration of caloric intake; use of water filtration devices or wood for boiling drinking water is not an option. Globally, unsafe water supplies, lack of sanitation, and poor hygiene practices continue to take a toll on public health and perpetuate the cycle of life-threatening, waterborne disease. According to recent WHO estimates, about 748 million people still lack access to a supply of improved drinking water, and 2.5 billion lack basic sanitation [5]. Rather than review burden and control of waterborne disease, which we have done quite recently [6, 7], this review will focus on some of the most immediate challenges facing the 21st century. Some are fundamental, such as failing infrastructure, where it exists, and the inability to educate people in some of the most basic tenets of hygiene and sanitation. Other challenges are in the realm of emerging diseases and the complexities of multiple infections from different agents, combined with chemical challenges, nutritional status, and other environmental health threats. Although beyond the scope of this article, geopolitical challenges remain the greatest barrier to control of waterborne disease on a global scale and will be discussed only briefly at the end of this paper. Infrastructure The pipes under our streets are old and leaky. It is not uncommon for utilities to estimate a loss of 30 % or more of the water flowing through a distribution system, and in some cases, losses can be much higher [8, 9]. Older piping may be laid adjacent to sewer lines, without today’s mandatory separation or casing requirements, making back siphonage of contaminated water a significant risk to human health [10]. Once contaminated, biofilms on pipe surfaces become a reservoir for a variety of pathogens, allowing certain pathogens to survive through provision of a protected environment, often in what has come to be known as a Bviable but non-culturable state^ [11, 12], and in some cases even allowing growth and proliferation for those pathogens considered Benvironmental^ [13, 14]. The corrosion literature is vast and would suggest that virtually no structural material is immune to fouling with the potential
Fig. 1 Copy of an original drawing of a three pot filtration system from Reginald Craufuird Sterndale in 1881 [3]
for biodeterioration [e.g., 15], which speaks to the massive problem that all countries face in relation to drinking water distribution systems. The estimated costs for replacing deteriorating systems are equally vast, and the task essentially impractical. Based on 2007 data, the US EPA [16] estimated that the US’ B53,000 community water systems and 21,400 not-for-profit noncommunity water systems will need to invest an estimated $334.8 billion between 2007 and 2027.^ Of this amount, transmission and distribution projects account for $200.8 billion of this cost. More recent analysts have suggested that upgrading both water and wastewater systems could cost in the trillions of dollars over the next 20 years [17]. Very few water systems could afford these levels of cost. The disruption to commerce in large cities is another important factor, and depending on water quality and piping materials, it is likely that many systems will need to start from the beginning again in 2027! The plastics industry suggests that PVC piping is the solution [e.g., 18], but even PVC may not be immune from biodeterioration [19]. Piping used after 1977 should not leach vinyl choride, a known carcinogen, but it is not clear whether the research is as yet conclusive [20], or the US EPA entirely agrees [21] (EPA 2012). The other problem is that organic chemicals such as gasoline weaken PVC and can even permeate the piping. Even if we were able to replace all galvanized pipe, unlined cast iron pipe, asbestos cement pipe, and ductile iron pipe with PVC (at far greater cost than $200 billion, we suspect), there will continue to be questions about its integrity. It is sobering to think about other countries with a fraction of
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the US GDP per capita (2013 estimate of $45,863 [22]. India, for example, which claims 30–50 % losses of water from its distribution systems has approximately one fortieth the US GDP per capita (known as nonrevenue water, these water loss estimates include leakage and other losses such as illegal connections [23].) Water distribution remains a necessity, and it is hard to envisage a system that does not involve vast networks of underground piping—for both water distribution and wastewater discharge. These investments will eventually have to be made, and at the same time, research will continue on more effective ways to keep drinking water safe, while minimizing potentially toxic disinfection by-products. Our understanding of biofilm microbiology, and particularly the concept that microbes signal to each other, is beginning to open up avenues for biofilm control. Disruption of these molecular mechanisms of aggregation, known as quorum sensing, has both environmental and therapeutic implications [24, 25]. It is hard to imagine adding a chemical to our drinking water that universally blocks quorum sensing, even if one could be found—and was nontoxic! However, the research has generated new ideas for evaluating biofilm formation and its control and could, for example, lead to future work on immobilizing quorum sensing blockers in materials at point of use [26], just as we impregnate filter materials with silver to inactivate pathogens [27]. Other opportunities for control may arise as we are increasingly able to identify genes that are expressed in dynamic Bbiofilm^ systems [e.g., 28]. In fact, we have come a long way in the past 20 years in our approaches to characterizing drinking water biofilms, from swabbing a faucet and streaking out samples on selective media, to a metagenomics approach. Although metagenomics has revolutionized our ability to rapidly describe microbial communities in both environmental and clinical samples [e.g., 29], it seems to have brought us no closer to solving fundamental questions about drinking water safety. Today, we can probably definitively detect the presence of specific virulence genes in drinking water biofilms, something suspected but hard to detect even 10 years ago—the early days of metagenomics [30]. The amazing sequencing technologies, together with bioinformatics tools such as GENIUS [31] to help us understand them, have resulted in extraordinary advances in the detection field, which clearly helps us in risk assessment from pathogens we have suspected for a long time, but the approach does not give us answers for control. We have discussed the issue of transfer of virulence and antibiotic genes within drinking water biofilms in a number of publications going back ~20 years or so [32, 33], yet can honestly state that the qualitative data on the microbiology of the drinking water biofilm remains a fascinating exercise of academic interest, but of little practical application. Our point here is that the next challenge is to translate scientific knowledge into practice—i.e., the environmental equivalent of Btranslational^ research.
Hygiene and Sanitation Why in the 21st century is this still an issue? With worldwide estimates of 1 billion people still practicing open defecation [34], many people continue to defecate where they drink. In addition, handwashing after defecation or other potential contact with fecal material remains a rarity. A recent review suggests that only 19 % of the world population practices handwashing with soap after potential contact with excreta, and in high income countries that number is still on average less than 50 % [35]. The data is not conclusive, but in this same study, a meta-regression of risk estimates suggests that handwashing could reduce the risk of diarrheal disease by 23 %, which is slightly lower than previous studies that suggested a reduction by 31 % of gastrointestinal disease and 21 % of respiratory disease [36]. This of course raises the old discourse of how clean is too clean? Are we in fact raising the relative risk of waterborne disease by reducing our own immunity through too much handwashing and use of soaps that may promote antibiotic resistance? There is actually a strong argument that we have already done that, particularly in high-income countries where there is now some push back against antimicrobial soaps and wipes [37]. There is little to no evidence that antimicrobial handwashing products are any more efficacious than those without antimicrobials, and their use may indeed be harmful in suppressing the bodies normal flora, promoting antimicrobial resistance, and causing ecological harm when discharged to the environment [38]. However, promoting use of nonantimicrobial soaps, with hygiene and sanitation education, remains undoubtedly one of the most effective ways to reduce spread of waterborne and other diseases. The key word here is education, and public health and other health professionals have done a poor job of conveying the message. Part of the reason is lack of community engagement. We still have the mindset that if we provide instruction and pamphlets to a community, they will understand and comply with the message. That simply is not the case [39]. In the last several years, community-based participatory research or CBPR has provided a more effective tool for dissemination of information. It is more of a social than a scientific construct and is focused on full community engagement in every area of the work, from basic research to health interventions. It should fully embrace both the cultural and environmental context of the intervention and is both initiated and implemented by community members rather than by external Baid workers^ [40]. Emerging Risks: Diarrheagenic Escherichia coli The recent emergence and evolution of novel strains of diarrheagenic Escherichia coli, especially the enterohemorrhagic E. coli (EHEC), are of increasing concern. The prototypic form of EHEC, serotype O157:H7, was first identified in
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human disease in 1982 [41]. Since then, disease outbreaks caused by O157:H7 and related EHEC serotypes have occurred at increasing frequency with increasing severity, with severity being defined by higher rates of hemolytic uremic syndrome (HUS) and hospitalization [42]. For example, the average frequency of HUS for 350 O157:H7 outbreaks occurring in the USA between 1982 and 2002 was 4 % [43]; a higher rate of HUS of 16 % was noted for the spinachassociated outbreak occurring in 2006 in California [44]. Newly emergent strains of non-EHEC but related and highly virulent diarrheagenic E. coli are also appearing. In 2011, serotype O104:H4 was responsible for an outbreak of diarrheal disease originating in Germany and affecting almost 4000 people; the outbreak included a high incidence of HUS and 54 deaths [45]. Similar to EHEC bacteria, the O104:H4 strain expressed Shiga toxin proteins, but was found to be a rare strain of enteroaggregative E. coli first identified in 2005 in a patient in South Korea [46]. The 2011 O104:H4 outbreak strain was described as being Bexceptionally virulent^ [45], causing HUS in 22 % of patients. The German O104:H4 strain was also unique in that it lacked the eae gene encoding the intimin adherence protein commonly expressed in EHEC infections. Monitoring and Surveillance of Escherichia coli Harboring Virulence Genes Our recent surveillance and tracking studies have examined the occurrence of the EHEC and related enteropathogenic E. coli (EPEC) in rivers of the Rocky Mountain region of the USA. Our findings suggest a widespread occurrence of strains harboring the eae gene characteristic of both EHEC and EPEC [47; Hamner and Ford, unpublished data]. As a teaching exercise for beginning biology students studying environmental and public health microbiology, we have introduced students in Montana and Colorado to water quality monitoring techniques, including enumeration and isolation of E. coli from local rivers, and screening isolates for the presence of disease-related genes, especially the eae gene. PCR testing of environmental bacteria for virulence genes demonstrates to students the practical application of molecular biology techniques to the study of public health and water quality issues in local neighborhoods. In a recent study of fecal contamination of the Little Bighorn River on the Crow Indian Reservation in southeast Montana, ten river isolates of EHEC bacteria were found to harbor virulence genes for both Shiga toxin and intimin proteins [47]. In our source tracking investigation of these bacteria, some 23 % of 167 manure isolates of E. coli were positive for the intimin gene. During 2013, as part of an introductory biology lab exercise, one strain of eae-positive EPEC was isolated by a student from her home ranch in a remote part of northern Montana. During 2014-15, our biology students found that 6 of their 72 isolates
of E. coli also tested positive for the eae gene; these bacteria were isolated from the Animus River flowing through Durango Colorado. Our experience of readily being able to isolate and identify putative EHEC and EPEC bacteria during teaching laboratory studies of water quality suggests that these bacteria have become widespread in the environment, notably in rural ranching communities. This should not be surprising, given that cattle are the primary reservoir of these bacteria and that high prevalence rates of EHEC in cattle herds have been frequently documented [48–50]. These and similar findings of environmental reservoirs for a variety of virulence genes in other bacterial species [51, 52] are worrisome. Many bacterial strains harboring a subset of virulence genes may not yet be pathogenic [52]. Acquisition of additional virulence genes from the environment via horizontal gene transfer raises the specter of evolution and emergence of more virulent bacterial strains in the future. The O104:H8 bacteria causing the 2011 outbreak in Germany is an example of just such a phenomenon. In this case, a virulent strain of enteroaggregative E. coli acquired additional genes found in Shiga toxin-expressing E. coli [45]. Reemerging Risks: Vibrio cholerae Ongoing study of cholera, an ancient disease long associated with the Gangetic plains and Bengal region of India, continues to reveal unexpected surprises and generate new insights about this particular disease as well as waterborne disease in general. Considered controversial at first, the discovery of Vibrio cholerae, the bacterium that causes cholera, in the Chesapeake Bay during the 1970s [53] led to our present understanding that these bacteria are found around the world in a variety of natural aquatic habitats [54] and are not spread solely by infected patients or through contamination by untreated sewage. In the natural environment, both pathogenic and nonpathogenic forms of the bacteria exist, often in association with copepods, shellfish, and aquatic plants. Nonpathogenic strains may possess some but not all of the virulence genes necessary to cause disease and may readily acquire additional genetic elements through horizontal gene transfer to become virulent [55]. Disease-related bacteria such as V. cholerae are constantly evolving during passage both in the host and in the environment, through the cumulative effects of mutation and gain and loss of genes coding for virulence factors [56]. Changes in expression and properties of specific virulence factors can lead to more serious disease. For example, analysis of recent clinical isolates of the O1 El Tor biotype from outbreaks in Bangladesh and Haiti has revealed the emergence of hypervirulent strains expressing unusually high levels of both cholera toxin and toxincoregulated pilus, the two major virulence factors associated with V. cholerae [57].
A Perspective on Waterborne Disease
The GENIUS bioinformatics/metagenomics analysis tool mentioned earlier [31] has recently been used in a study involving the National Institute of Cholera and Enteric Diseases (NICED) in Bangladesh to examine the profiles of pathogenic bacteria found in cholera patients [58]. In conjunction with traditional diagnostic, culture techniques, GENIUS analysis has confirmed the presence of both V. cholerae bacteria and strains of Shigella and/or Salmonella in one subset of cholera patients, while confirming the absence of V. cholerae bacteria but the presence of Shigella or EPEC bacteria in another subset of presumed cholera patients [58]. Application of such a powerful bioinformatics approach may force a redefinition of how cholera is diagnosed and/or treated.
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Geopolitical 8.
It has been 20 years since then Vice President of the World Bank, Ismail Seregeldin, talked about the possibility that the wars of the next century will be fought over water (as opposed to oil, August 1995 [59]). This sentiment has been reiterated many times since then, at times citing Seregeldin, at other times framed as a new idea! In fact, conflicts have been fought over water, and water has been used as a military tool, for thousands of years (see Pacific Institute for a timeline [60]). The reality today is that population pressures, water scarcity, and unequal distribution of resources have never been as extreme, and are projected to only worsen over the coming decades with climate change, continued population growth, movement, and conflict. Water is extensively being used as an instrument of war by all sides in the current conflicts in Syria and Iraq. These are two countries that already face water stress and scarcity, fueled in part by Turkey’s dam and hydropower construction [61]. Whatever national and international policies we put in place, water will always be an incredibly powerful military tool. We have only to look at why fighting has been so intense around Iraq’s largest dams, the Mosul and Haditha dams. Whoever controls these resources, controls much of the country’s irrigation and electricity [62]. Water resources will always be used as a military tool, that, regrettably is human nature. The challenge for the future is to minimize water scarcity so that water no longer becomes an excuse for conflict.
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Colwell RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274:2025–2031 55. Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301–1314, PMCID: PMC98947 56. Dolores J, Satchell KJF (2013) Analysis of Vibrio cholerae genomic sequences reveals unique rtxA variants in environmental strains and an rtxA-null mutation in recent El Tor isolates. MBio 4(2): e00624. doi:10.1128/mBio.00624-12, PMCID: PMC3634609 57. Son MS, Megli CJ, Kovacikova G, Qadri F, Taylor RK (2011) Characterization of Vibrio cholerae O1 El Tor biotype variant clinical isolates from Bangladesh and Haiti, including a molecular genetic analysis of virulence genes. J Clin Microbiol 49:3739–3749, PMCID: PMC3209127
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Colwell RR (2014) Climate change, oceans, and infectious disease: Cholera pandemics as a model. Society for General Microbiology Annual Conference, April 2014. https://www. youtube.com/watch?v=KvBuDxwV11Y (accessed December 2014.) Serageldin I (2014). http://www.serageldin.com/Water.htm Pacific Institute. http://www2.worldwater.org/conflict/list/ Haftendorn H (2000) Water and international conflict. Third World Q 21:51–68 Cunningham E (2014) Islamic State jihadists are using water as a weapon in Iraq. The Washington Post. October 7, 2014. http:// www.washingtonpost.com/world/middle_east/islamic-statejihadists-are-using-water-as-a-weapon-in-iraq/2014/10/06/ aead6792-79ec-4c7c-8f2f-fd7b95765d09_story.html
SHORT COMMENTARY
A Perspective on the Global Pandemic of Waterborne Disease Timothy E Ford 1 & Steve Hamner 2
Received: 13 January 2015 / Accepted: 14 May 2015 # Springer Science+Business Media New York 2015
Abstract Waterborne diseases continue to take a heavy toll on the global community, with developing nations, and particularly young children carrying most of the burden of morbidity and mortality. Starting with the historical context, this article explores some of the reasons why this burden continues today, despite our advances in public health over the past century or so. While molecular biology has revolutionized our abilities to define the ecosystems and etiologies of waterborne pathogens, control remains elusive. Lack of basic hygiene and sanitation, and failing infrastructure, remain two of the greatest challenges in the global fight against waterborne disease. Emerging risks continue to be the specter of multiple drug resistance and the ease with which determinants of virulence appear to be transmitted between strains of pathogens, both within and outside the human host. Keywords Hygiene . Sanitation . Infrastructure . Pathogens . Biofilms . Sequencing . E. coli
Introduction In order to present a perspective, it is important to look back through history to see how far we have come in the global fight against waterborne disease. I (Ford) am fortunate to be able to do that on a personal level, although my conclusion is that we have not come very far—at least in combatting diseases * Timothy E Ford [email protected] 1
School of Health Professions, Shenandoah University, Winchester, VA 22601, USA
2
Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
transmitted through contaminated drinking water in less developed countries. In his journals, my great ×4 grandfather wrote: BThe Cholera very much in progress – many victims here 30 or 40 in Jennings’ Buildings [a notorious slum off Kensington High Street, TF]. Salt particularly recommend to be used in small quantities for the cholera – a statement in the Spectator states this at full length & complains, justly, of the monopoly of the East India Company preventing the Natives enjoying this necessary healthy comfort & attributes the Cholera very much to this deprivation.^ Jonathan Bell, Kensington, London, January 1849. The Bstatement^ to which he refers is most likely Brown 1849 [1], which even today makes compelling reading. Although the mechanism discussed at the time was very different from the one we know today, oral rehydration therapy, at least the replenishment of salts is not completely an idea of the past 45 years or so [2]. What about the widely adopted low-cost water filtration systems that abound today? Again, I am informed by my predecessors, in this case my great ×2 grandfather, Reginald Craufuird Sterndale, who both wrote about and illustrated the basic process in 1881 [3]. At the time, he was Vice Chairman of the municipality of the suburbs of Calcutta and would later become Cantonment Magistrate, Dum Dum. To quote: BThere can be no doubt that, if the people could be induced to boil and filter the water used by them, that many dangerous waters might be thus used with comparative safety; but this cannot be expected, the very cost of fuel would prevent the poorer classes from taking this precaution; nor is it probably that they could, to any
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extent be brought to filter their drinking water, although materials for constructing a most efficient filter is to their hand, and at an outlay of but a few pice (former monetary unit) – a rough wooden stand, three ordinary porous earthenware culshis or jars, a small quantity of charcoal or sand being all that is necessary.^ Fig. 1. More than a century later, this situation remains unchanged for the world’s poorest citizens. During our 2004 study of water use patterns practiced by residents of Varanasi India, those interviewed reported using the heavily polluted Ganges River for everyday washing of dishes and laundry, personal hygiene, and as a primary source of drinking water [4]. The poorest among these residents devote their daily existence to procuring another day’s ration of caloric intake; use of water filtration devices or wood for boiling drinking water is not an option. Globally, unsafe water supplies, lack of sanitation, and poor hygiene practices continue to take a toll on public health and perpetuate the cycle of life-threatening, waterborne disease. According to recent WHO estimates, about 748 million people still lack access to a supply of improved drinking water, and 2.5 billion lack basic sanitation [5]. Rather than review burden and control of waterborne disease, which we have done quite recently [6, 7], this review will focus on some of the most immediate challenges facing the 21st century. Some are fundamental, such as failing infrastructure, where it exists, and the inability to educate people in some of the most basic tenets of hygiene and sanitation. Other challenges are in the realm of emerging diseases and the complexities of multiple infections from different agents, combined with chemical challenges, nutritional status, and other environmental health threats. Although beyond the scope of this article, geopolitical challenges remain the greatest barrier to control of waterborne disease on a global scale and will be discussed only briefly at the end of this paper. Infrastructure The pipes under our streets are old and leaky. It is not uncommon for utilities to estimate a loss of 30 % or more of the water flowing through a distribution system, and in some cases, losses can be much higher [8, 9]. Older piping may be laid adjacent to sewer lines, without today’s mandatory separation or casing requirements, making back siphonage of contaminated water a significant risk to human health [10]. Once contaminated, biofilms on pipe surfaces become a reservoir for a variety of pathogens, allowing certain pathogens to survive through provision of a protected environment, often in what has come to be known as a Bviable but non-culturable state^ [11, 12], and in some cases even allowing growth and proliferation for those pathogens considered Benvironmental^ [13, 14]. The corrosion literature is vast and would suggest that virtually no structural material is immune to fouling with the potential
Fig. 1 Copy of an original drawing of a three pot filtration system from Reginald Craufuird Sterndale in 1881 [3]
for biodeterioration [e.g., 15], which speaks to the massive problem that all countries face in relation to drinking water distribution systems. The estimated costs for replacing deteriorating systems are equally vast, and the task essentially impractical. Based on 2007 data, the US EPA [16] estimated that the US’ B53,000 community water systems and 21,400 not-for-profit noncommunity water systems will need to invest an estimated $334.8 billion between 2007 and 2027.^ Of this amount, transmission and distribution projects account for $200.8 billion of this cost. More recent analysts have suggested that upgrading both water and wastewater systems could cost in the trillions of dollars over the next 20 years [17]. Very few water systems could afford these levels of cost. The disruption to commerce in large cities is another important factor, and depending on water quality and piping materials, it is likely that many systems will need to start from the beginning again in 2027! The plastics industry suggests that PVC piping is the solution [e.g., 18], but even PVC may not be immune from biodeterioration [19]. Piping used after 1977 should not leach vinyl choride, a known carcinogen, but it is not clear whether the research is as yet conclusive [20], or the US EPA entirely agrees [21] (EPA 2012). The other problem is that organic chemicals such as gasoline weaken PVC and can even permeate the piping. Even if we were able to replace all galvanized pipe, unlined cast iron pipe, asbestos cement pipe, and ductile iron pipe with PVC (at far greater cost than $200 billion, we suspect), there will continue to be questions about its integrity. It is sobering to think about other countries with a fraction of
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the US GDP per capita (2013 estimate of $45,863 [22]. India, for example, which claims 30–50 % losses of water from its distribution systems has approximately one fortieth the US GDP per capita (known as nonrevenue water, these water loss estimates include leakage and other losses such as illegal connections [23].) Water distribution remains a necessity, and it is hard to envisage a system that does not involve vast networks of underground piping—for both water distribution and wastewater discharge. These investments will eventually have to be made, and at the same time, research will continue on more effective ways to keep drinking water safe, while minimizing potentially toxic disinfection by-products. Our understanding of biofilm microbiology, and particularly the concept that microbes signal to each other, is beginning to open up avenues for biofilm control. Disruption of these molecular mechanisms of aggregation, known as quorum sensing, has both environmental and therapeutic implications [24, 25]. It is hard to imagine adding a chemical to our drinking water that universally blocks quorum sensing, even if one could be found—and was nontoxic! However, the research has generated new ideas for evaluating biofilm formation and its control and could, for example, lead to future work on immobilizing quorum sensing blockers in materials at point of use [26], just as we impregnate filter materials with silver to inactivate pathogens [27]. Other opportunities for control may arise as we are increasingly able to identify genes that are expressed in dynamic Bbiofilm^ systems [e.g., 28]. In fact, we have come a long way in the past 20 years in our approaches to characterizing drinking water biofilms, from swabbing a faucet and streaking out samples on selective media, to a metagenomics approach. Although metagenomics has revolutionized our ability to rapidly describe microbial communities in both environmental and clinical samples [e.g., 29], it seems to have brought us no closer to solving fundamental questions about drinking water safety. Today, we can probably definitively detect the presence of specific virulence genes in drinking water biofilms, something suspected but hard to detect even 10 years ago—the early days of metagenomics [30]. The amazing sequencing technologies, together with bioinformatics tools such as GENIUS [31] to help us understand them, have resulted in extraordinary advances in the detection field, which clearly helps us in risk assessment from pathogens we have suspected for a long time, but the approach does not give us answers for control. We have discussed the issue of transfer of virulence and antibiotic genes within drinking water biofilms in a number of publications going back ~20 years or so [32, 33], yet can honestly state that the qualitative data on the microbiology of the drinking water biofilm remains a fascinating exercise of academic interest, but of little practical application. Our point here is that the next challenge is to translate scientific knowledge into practice—i.e., the environmental equivalent of Btranslational^ research.
Hygiene and Sanitation Why in the 21st century is this still an issue? With worldwide estimates of 1 billion people still practicing open defecation [34], many people continue to defecate where they drink. In addition, handwashing after defecation or other potential contact with fecal material remains a rarity. A recent review suggests that only 19 % of the world population practices handwashing with soap after potential contact with excreta, and in high income countries that number is still on average less than 50 % [35]. The data is not conclusive, but in this same study, a meta-regression of risk estimates suggests that handwashing could reduce the risk of diarrheal disease by 23 %, which is slightly lower than previous studies that suggested a reduction by 31 % of gastrointestinal disease and 21 % of respiratory disease [36]. This of course raises the old discourse of how clean is too clean? Are we in fact raising the relative risk of waterborne disease by reducing our own immunity through too much handwashing and use of soaps that may promote antibiotic resistance? There is actually a strong argument that we have already done that, particularly in high-income countries where there is now some push back against antimicrobial soaps and wipes [37]. There is little to no evidence that antimicrobial handwashing products are any more efficacious than those without antimicrobials, and their use may indeed be harmful in suppressing the bodies normal flora, promoting antimicrobial resistance, and causing ecological harm when discharged to the environment [38]. However, promoting use of nonantimicrobial soaps, with hygiene and sanitation education, remains undoubtedly one of the most effective ways to reduce spread of waterborne and other diseases. The key word here is education, and public health and other health professionals have done a poor job of conveying the message. Part of the reason is lack of community engagement. We still have the mindset that if we provide instruction and pamphlets to a community, they will understand and comply with the message. That simply is not the case [39]. In the last several years, community-based participatory research or CBPR has provided a more effective tool for dissemination of information. It is more of a social than a scientific construct and is focused on full community engagement in every area of the work, from basic research to health interventions. It should fully embrace both the cultural and environmental context of the intervention and is both initiated and implemented by community members rather than by external Baid workers^ [40]. Emerging Risks: Diarrheagenic Escherichia coli The recent emergence and evolution of novel strains of diarrheagenic Escherichia coli, especially the enterohemorrhagic E. coli (EHEC), are of increasing concern. The prototypic form of EHEC, serotype O157:H7, was first identified in
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human disease in 1982 [41]. Since then, disease outbreaks caused by O157:H7 and related EHEC serotypes have occurred at increasing frequency with increasing severity, with severity being defined by higher rates of hemolytic uremic syndrome (HUS) and hospitalization [42]. For example, the average frequency of HUS for 350 O157:H7 outbreaks occurring in the USA between 1982 and 2002 was 4 % [43]; a higher rate of HUS of 16 % was noted for the spinachassociated outbreak occurring in 2006 in California [44]. Newly emergent strains of non-EHEC but related and highly virulent diarrheagenic E. coli are also appearing. In 2011, serotype O104:H4 was responsible for an outbreak of diarrheal disease originating in Germany and affecting almost 4000 people; the outbreak included a high incidence of HUS and 54 deaths [45]. Similar to EHEC bacteria, the O104:H4 strain expressed Shiga toxin proteins, but was found to be a rare strain of enteroaggregative E. coli first identified in 2005 in a patient in South Korea [46]. The 2011 O104:H4 outbreak strain was described as being Bexceptionally virulent^ [45], causing HUS in 22 % of patients. The German O104:H4 strain was also unique in that it lacked the eae gene encoding the intimin adherence protein commonly expressed in EHEC infections. Monitoring and Surveillance of Escherichia coli Harboring Virulence Genes Our recent surveillance and tracking studies have examined the occurrence of the EHEC and related enteropathogenic E. coli (EPEC) in rivers of the Rocky Mountain region of the USA. Our findings suggest a widespread occurrence of strains harboring the eae gene characteristic of both EHEC and EPEC [47; Hamner and Ford, unpublished data]. As a teaching exercise for beginning biology students studying environmental and public health microbiology, we have introduced students in Montana and Colorado to water quality monitoring techniques, including enumeration and isolation of E. coli from local rivers, and screening isolates for the presence of disease-related genes, especially the eae gene. PCR testing of environmental bacteria for virulence genes demonstrates to students the practical application of molecular biology techniques to the study of public health and water quality issues in local neighborhoods. In a recent study of fecal contamination of the Little Bighorn River on the Crow Indian Reservation in southeast Montana, ten river isolates of EHEC bacteria were found to harbor virulence genes for both Shiga toxin and intimin proteins [47]. In our source tracking investigation of these bacteria, some 23 % of 167 manure isolates of E. coli were positive for the intimin gene. During 2013, as part of an introductory biology lab exercise, one strain of eae-positive EPEC was isolated by a student from her home ranch in a remote part of northern Montana. During 2014-15, our biology students found that 6 of their 72 isolates
of E. coli also tested positive for the eae gene; these bacteria were isolated from the Animus River flowing through Durango Colorado. Our experience of readily being able to isolate and identify putative EHEC and EPEC bacteria during teaching laboratory studies of water quality suggests that these bacteria have become widespread in the environment, notably in rural ranching communities. This should not be surprising, given that cattle are the primary reservoir of these bacteria and that high prevalence rates of EHEC in cattle herds have been frequently documented [48–50]. These and similar findings of environmental reservoirs for a variety of virulence genes in other bacterial species [51, 52] are worrisome. Many bacterial strains harboring a subset of virulence genes may not yet be pathogenic [52]. Acquisition of additional virulence genes from the environment via horizontal gene transfer raises the specter of evolution and emergence of more virulent bacterial strains in the future. The O104:H8 bacteria causing the 2011 outbreak in Germany is an example of just such a phenomenon. In this case, a virulent strain of enteroaggregative E. coli acquired additional genes found in Shiga toxin-expressing E. coli [45]. Reemerging Risks: Vibrio cholerae Ongoing study of cholera, an ancient disease long associated with the Gangetic plains and Bengal region of India, continues to reveal unexpected surprises and generate new insights about this particular disease as well as waterborne disease in general. Considered controversial at first, the discovery of Vibrio cholerae, the bacterium that causes cholera, in the Chesapeake Bay during the 1970s [53] led to our present understanding that these bacteria are found around the world in a variety of natural aquatic habitats [54] and are not spread solely by infected patients or through contamination by untreated sewage. In the natural environment, both pathogenic and nonpathogenic forms of the bacteria exist, often in association with copepods, shellfish, and aquatic plants. Nonpathogenic strains may possess some but not all of the virulence genes necessary to cause disease and may readily acquire additional genetic elements through horizontal gene transfer to become virulent [55]. Disease-related bacteria such as V. cholerae are constantly evolving during passage both in the host and in the environment, through the cumulative effects of mutation and gain and loss of genes coding for virulence factors [56]. Changes in expression and properties of specific virulence factors can lead to more serious disease. For example, analysis of recent clinical isolates of the O1 El Tor biotype from outbreaks in Bangladesh and Haiti has revealed the emergence of hypervirulent strains expressing unusually high levels of both cholera toxin and toxincoregulated pilus, the two major virulence factors associated with V. cholerae [57].
A Perspective on Waterborne Disease
The GENIUS bioinformatics/metagenomics analysis tool mentioned earlier [31] has recently been used in a study involving the National Institute of Cholera and Enteric Diseases (NICED) in Bangladesh to examine the profiles of pathogenic bacteria found in cholera patients [58]. In conjunction with traditional diagnostic, culture techniques, GENIUS analysis has confirmed the presence of both V. cholerae bacteria and strains of Shigella and/or Salmonella in one subset of cholera patients, while confirming the absence of V. cholerae bacteria but the presence of Shigella or EPEC bacteria in another subset of presumed cholera patients [58]. Application of such a powerful bioinformatics approach may force a redefinition of how cholera is diagnosed and/or treated.
3.
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7.
Geopolitical 8.
It has been 20 years since then Vice President of the World Bank, Ismail Seregeldin, talked about the possibility that the wars of the next century will be fought over water (as opposed to oil, August 1995 [59]). This sentiment has been reiterated many times since then, at times citing Seregeldin, at other times framed as a new idea! In fact, conflicts have been fought over water, and water has been used as a military tool, for thousands of years (see Pacific Institute for a timeline [60]). The reality today is that population pressures, water scarcity, and unequal distribution of resources have never been as extreme, and are projected to only worsen over the coming decades with climate change, continued population growth, movement, and conflict. Water is extensively being used as an instrument of war by all sides in the current conflicts in Syria and Iraq. These are two countries that already face water stress and scarcity, fueled in part by Turkey’s dam and hydropower construction [61]. Whatever national and international policies we put in place, water will always be an incredibly powerful military tool. We have only to look at why fighting has been so intense around Iraq’s largest dams, the Mosul and Haditha dams. Whoever controls these resources, controls much of the country’s irrigation and electricity [62]. Water resources will always be used as a military tool, that, regrettably is human nature. The challenge for the future is to minimize water scarcity so that water no longer becomes an excuse for conflict.
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