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CHAPTER 1

Introduction

Jamie Bartram

The excreta (faeces and urine) of mammals and birds are widespread across planet Earth (Figure 1.1) and frequently contaminate water used for bathing and recreation, for treatment and distribution for human consumption, and for irrigating crops.

The risk that such contamination represents to human health is inadequately understood. It is widely assumed that animal faeces represents a lesser risk to human health than human faeces, because of the "species barrier" and especially the species-specificity of most viruses. This assumption has had important consequences for the selection and prioritization of remedial interventions. For example, studies on the impact of faecally-contaminated coastal "waters on the health of bathers" often report symptoms that are consistent with viral aetiology. Species-specificity among viruses indicates an association with human faeces and a priority focus on reducing sewage pollution where this is occurs.

There is at least some cause for concern about contamination of waters with animal excreta, as animal to human waterborne transmission has been documented for several pathogens. Waterborne transmission of E. coli O157 has been repeatedly documented and has been associated with outbreaks, including cases of haemolytic uremic syndrome (HUS), especially through drinking-water and to a lesser extent recreational water use. In one outbreak in Swaziland cattle manure was thought to be the source of more than 40, 000 cases of waterborne infection with the organism (Effler et al. 2001). One study (Wilson et al. 2008) concluded that 96.6% of human clinical infections with Campylobacter jejuni in Lancashire, UK could be attributed to farm livestock. Animal reservoir hosts play an important role in the transmission of Schistosoma japonicum in both China and the Philippines, with a high level of transmission between species, although evidence suggests that different animal species are important in the two countries (see Chapter 2 and a case study in Chapter 4).

There may be "win-win" opportunities with net economic benefits in better regulation of animal excreta. These arise from the potential to reduce human disease, improve animal health and recover the energy and nutrient value embedded in this resource – which is largely treated as waste at present. These benefits are most readily achievable in more concentrated operations such as large animal feedlots.

Many of the tools that have been used in assessing, managing and regulating risks to human health from contamination of water with human faeces are not applicable, or require adaptation for application, to the control of contamination by animal faeces. As examples: the relationship between the measurements of faecal indicator bacteria that have been used to index the health risk from faecal contamination are derived for sewage-polluted waters and unlikely to be applicable to waters where faecal pollution is significantly non-human in origin. Similarly, while the discipline of microbial risk assessment is advancing rapidly, data to support its application to organisms of zoonotic origin are limited; lack of adequate exposure measures effectively precludes prospective epidemiological studies.

Much of the management and regulatory experience that has been accrued from the control of human excreta is also directly transferable to management of animal waste. Livestock sources are mostly diffuse (e.g. fresh faeces or stored manures applied to land), though some point sources occur (cattle feedlots, manure heaps, etc.) and have variable characteristics, depending on local conditions.

These challenges and opportunities are compounded by differences between correct and incorrect risk perceptions among the general public, professionals and regulators alike, that are likely to be substantive.

During the consultations that led to the preparation of this publication examples were encountered of both over-confidence in the protection afforded by the "species barrier" and of concern driven by alarmist description of risk. For example, the suggestion that gastroenteritis among swimmers and animal non-point source contaminated water were "not associated" (Calderon et al. 1991) has been disputed (McBride 1993) and indeed in a subsequent review USEPA concluded

"Thus, water bodies with substantial animal inputs can result in potential human health risks on par with those that result from human faecal inputs." (EPA, 2011 lines 1605–1607).

One anecdote described a country in which responsibility for control of campylobacteriosis was transferred from the Health to the Food Safety authority, whose policy makers then asserted that Campylobacter could not be waterborne, because it is foodborne. Of course it is both, and to exclude the waterborne component would inadequately protect public health (see for example McBride et al. (2011)).

1.1 PROBLEM DESCRIPTION

There is a mismatch between present regulatory approaches and the needs of effective health protection against the potential risks from water-related zoonotic hazards. There is no specific guidance available on the assessment of risks arising from contamination of waters by animal faeces; nor on the development of health criteria for waters contaminated by animal faeces. This initiative is therefore driven by two pressures: regulatory and risk (including perceived risk).

This will be the second book in the series on "Emerging issues in water and infectious disease" to deal with issues related to zoonoses; in part in recognition of the fact that the majority, around 75%, of emerging and re-emerging pathogens are zoonotic. The first book, "Water-borne Zoonoses" (Cotruvo et al. 2004), which complements this volume, focused on three questions:

• The nature of waterborne zoonotic disease threats;

• Identification of new disease candidates; and,

• Adequacy of existing control measures.

In contrast this volume focuses on:

• The adequacy of the evidence base for policy;

• The appropriateness and effectiveness of present regulatory responses; and,

• Opportunities for effective low-cost regulation and management of actual and potential health risks.

For the purposes of assessment, management and regulation, the issue consists of three principal components: the source (animal excreta), its transport (i.e. transfer to, survival in and movement through watercourses); and resulting human exposure. All three can be the object of interventions.

This report, therefore, reflects on understanding what are the assessment, managerial and regulatory challenges, the adequacy of present regulatory approaches, and the characteristics of a better system.

For bathing waters the established approach was, for many years, retrospective compliance testing on an annual basis. However the 1999 "Annapolis Protocol" (WHO, 1999), associated World Health Organization's Guidelines (WHO 2003; 2006) and their implementation in associated developments (EU, New Zealand 2003) show a strong shift towards prevention and real-time support for informed decision-making by members of the public. These documents also recognize, however, that health risks from zoonotic sources in absolute terms or as compared with faecal indicators are inadequately understood and they are cautious in interpreting the associated risks, except in assuming that the risk presented by animal excreta is less than that from human excreta.

For drinking-water the shift to preventive management is more advanced, with detectable changes in regulation and/or practice since the publication of the third edition of WHO's Guidelines for Drinking-water Quality which recommended a "Framework for Drinking-water Safety" and associated "Water Safety Plans" (WHO 2004, reconfirmed in the fourth edition, WHO 2011). However, problems remain of inadequate understanding of zoonotic risks and the inadequacy of faecal bacteria as indicators of risk.

In the case of wastewater use in agriculture, preventive management approaches have been long-advocated to control the risks associated with introducing human excreta, and also effluents and sludge derived from sewage processing, into food production systems (WHO 1973; WHO 1989 and, more recently, with a multi-barrier approach, WHO, 2006b). In deriving these guidelines no account has been taken, however, of potential hazards in mixed wastes where human and animal excreta are both present; and there have been no substantive efforts targeted specifically on animal waste.

All of these routes of human exposure (recreational water use, drinking-water consumption and food produce grown with animal excreta inputs) have the potential to transmit a range of hazards including pathogens (micro-organisms capable of causing disease in humans) and toxic chemicals, including heavy metals and pharmaceuticals, including drugs, antibiotics and their residues. Antibiotics and chemicals used in animal care are of concern but are not separately addressed here. Available evidence suggests that the risks to human health are overwhelmingly dominated by microbial pathogens, and interrupting their transmission is therefore the focus of this book.

1.2 CHALLENGES

Available evidence suggests that risk associated with animal excreta is likely to be episodic in nature. This may arise because of sporadic load (e.g. migrating bird flocks) or sporadic transmission (e.g. mobilization of material on the ground surface or from water sediments following rainfall). Further complexity is added by the extreme spatial and temporal variability arising from factors such as seasonal weather patterns, livestock operations management (e.g. washing out of cattle sheds, seasonal grazing) as well as cycles of calving and associated microbial colonization and shedding including the phenomenon of "super-shedders" among herds and flocks. In New Zealand for example, at times of low river flow, Campylobacter isolates are primarily of ovine origin while strains of bovine origin dominate at times of high river flow.

Several studies have quantified the relative impacts of sewage and animal derived fluxes of microbial pollution to bathing waters (Stapleton et al. 2008, 2010; Kay et al. 2009; 2010; 2012). In an early study of rural catchments, Crowther et al. (2002) report on two such studies in the United Kingdom. Both catchments were livestock farming areas and the streams draining these areas were considered "pristine" in ecological terms. In both areas, bathing water quality noncompliance occurred after rainfall events. Studies revealed that this noncompliance was caused by microbial pollution from "normal" farming activities. Sewerage was not a significant cause of non-compliance during dry weather conditions when anthropogenic load dominated. A similar pattern was reported by Stapleton et al. (2010). Again, livestock-derived, microbial flux dominated during periods of rainfall and improvements to water quality during this period from investments in sewerage systems were imperceptible. In this case, water quality was key to microbial compliance of adjacent shellfish-harvesting waters.

Many of the species of pathogens of concern are circulating naturally within one animal species or the other or among humans, and there may be significant strain or species specificity. Thus, simple and conventional classification and categorization of microbes may be misleading; and criteria based on aggregate microbial groupings may significantly under- or over-estimate risk. Similarly a single water body may be contaminated by faeces from different animal species and this contamination may contain strains of the same micro-organism from different host species. These factors all add complexity to the assessment of risk and to the management and regulation of water contamination with animal excreta.

These complexities highlight some of the demands on risk assessment practice. Neither available tools nor data can adequately respond to the associated challenges. Most available data, for example on the effectiveness of interventions, relate to faecal indicator bacteria (such as E coli, thermotolerant coliforms or intestinal enterococci) and not to pathogens. These faecal indicator bacteria are imperfect measures or indicators of pathogen die-off. Nevertheless, systematic monitoring of zoonotic pathogens in the environment is rare. Much risk assessment practice focuses primarily on steady state conditions but, in fact, zoonotic risk is likely to be very episodic and variable. Similarly, most risk assessment is based on impacts on numbers of individuals, not dynamically on populations (disease dynamics) and there is increasing recognition of the inadequacy of such approaches for the above reasons.

These complexities also point to challenges for effective regulation. For example, present regulatory approaches may permit sporadic failure, especially when associated with extreme events. However, targeting regulation on health risk would mean recognizing that such episodes may represent the periods of greatest risk that should, in fact, be targeted by regulation. A further challenge in assembling an effective portfolio of regulatory measures is that its elements may be many and diverse. Distinct components may be direct (for example, targeted on agricultural practices or land use planning) or indirect (for example, food standards requiring irrigation water quality standards or best practice in manure use in agriculture). Securing a consistent approach that is effective and not onerous or costly across the multiple potential legal instruments that may apply in any given jurisdiction will not be easy. Similarly, while there is extensive experience with regulating point sources of pollution in many jurisdictions, regulation targeting microbial movement is relatively new and lessons are still being learned; and there is little substantive experience with regulation targeting human exposure.

At the interface of narrowly-defined regulation and wider policy, and including arrangements for inter-sectoral coordination, are the differing perspectives of the individual facility or farm and the collective impact of many such facilities or farms on a single catchment, including its multiple and diverse uses and the value and utility of such uses – extending into the associated coastal zone. This also implies an understanding of overall microbial load and of associated health risks (Kay et al. 2004).

Benefit-cost analysis (BCA) is one means to pursue regulatory efficiency, by demanding that both costs and benefits be described and to the extent possible quantified; and using the evidence derived to compare alternative responses and to reflect on means to minimize cost and maximize benefits of adopted approaches (Hahn & Tetlock 2008). Application of BCA to livestock excreta management for health protection has not been attempted in large part because benefits are poorly understood. For example, many interventions will operate on a number of pathogens and not a single agent. The outbreak of waterborne disease in Walkerton, Ontario, Canada that resulted in seven deaths and over 2300 cases of gastrointestinal illness was associated with infections by both E. coli O157:H7 and Campylobacter jejuni. Intense rainfall is thought to have washed cattle manure into a well which served as the water source for the town (Auld, Klaassen & Geast 2001). The nature of benefits is also evolving as greater attention is given to energy and nutrient recovery; and as the appreciation of the value of the recovered resources increases, so the benefit component of BCA expands accordingly.

(Continues…)

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Excerpted from "Animal Waste, Water Quality and Human Health"
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Copyright © 2012 World Health Organization.
Excerpted by permission of IWA Publishing.
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