6. Public Health and Livestock-Fish

The public health implications of livestock-fish integration are investigated in this chapter. Many of these are as important for specialized, stand-alone livestock and fish production as for integrated systems. Historical associations between human health and livestock production are compared to modern threats and how a large range of inputs to livestock, fish and wider food production systems may impact directly or indirectly on public health. Identifying the hazards and assessing the risks of pathogens including bacteria and viruses and parasites, are considered, and the involvement of integrated farming in influenza pandemics is discussed.

The importance of both chemical and biological hazards is raised. The current debate about anti-microbial resistance is interpreted from the standpoint of extra risk due to integration. Relative risks from bioaccumulation and toxic algal blooms are discussed.

6.1 General Considerations

Public health issues can be considered as those of direct importance to both producers and consumers of fish and include broader issues of food production, processing and delivery systems. Linkages have been made between fish or livestock production and health in terms of communicable diseases, non-communicable disease, malnutrition and injury (Birley and Lock, 1998). Clearly, the improved availability of low-cost fish and livestock products for people’s nutrition needs to be placed in perspective with likely risks.

Threats to public health from both livestock and aquaculture are diverse. Recently, livestock and fish have been implicated in the irregular occurrence of influenza pandemics; the global impacts on public health of promoting livestock and fish integration are huge if these claims are substantiated. Certainly throughout history, infectious diseases have largely entered human populations through animals (Morse, 1990). It has been known for some time, that common pathogens of warm-blooded animals do not generally cause disease in fish (Guelin, 1962 cited by Buras, 1990), but the role of cultured fish in the possible transfer of pathogens between livestock and humans is important, particularly in less developed countries.

Producers and consumers in developed countries are not immune, however, as the increasing number of food scares indicates and the global food trade continues to expand. Both the resurgence of ‘old’ risks, such as the recent outbreaks of anthrax in Australia and Thailand, and newly identified problems such as BSE in the UK show the interconnection between the health of humans and their food. The recently identified problem of Streptococcus iniae in tilapia in North America also raises the spectre of food hygiene becoming a major political issue, complicating the promotion of new aquaculture species by new producers.

Livestock and fish are involved in both passive and active transfer of a range of parasites and diseases to humans, broadening the need for risk assessment. The role of fish and warm-blooded livestock as intermediate hosts for a range of human parasites and control strategies are well known. However, the increasing use of a range of technologies, chemicals and feed ingredients in both livestock and fish production poses a relatively new set of risks. Products such as antimicrobials, pesticides and a range of chemotheropeutants are often used with little idea of either indirect or long-term risks. Prophylactic use of antibiotics and growth promoters in intensive fish feeds rival their use in the livestock industry. Similar problems, in terms of public health and consumer resistance, have arisen with legislation governing the use of these compounds in different countries threatening international trade. The development of genetically modified organisms, either as feeds of livestock and fish, or the animals themselves has been raised as both a moral and public health issue.

A holistic, balanced assessment of risks involved with integrated livestock-fish production needs to consider the alternative and more specialized, separate intensive systems. An example is the impact of livestock and fish culture on water quality as independent or integrated activities. Pollution of surface and ground water, with direct negative impacts on health may be avoided if wastes are recycled through integrated aquaculture with little to no impacts. The pooling of water has often been related to the spread of insect-vector borne diseases but use of water for aquaculture may reduce this risk. Unmanaged water bodies in rural or peri-urban areas are more likely to harbour suitable micro-habitats for hosts’ pests than ponds stocked and managed for fish culture. Adoption of livestock wastes for use in fish culture may already have made important contributions to improving health and hygiene. In Taiwan, economic growth with improved sanitation and increasing livestock production have led to replacement of human waste with pig and poultry manure as fertilizers in fish culture over the last few decades.

Risk analysis, in which hazards are identified and their relevance and control methods determined, is a logical approach to assessing the implications of integrating livestock and fish production on public health. An attempt is made to identify the hazards associated with the various practices constituting integrated livestock-fish and the risks associated with them.

6.1.1 PATHOGENS

Pathogens can affect human health through both active and passive contact. There are potential risks from handling livestock and their feeds, their production and slaughter house wastes as occur in stand-alone livestock farming. In addition there is a need to consider hazards associated with transfer and use of wastes for fish culture, in management, harvest and marketing of fish, and in addition, potential risks involved with preparing and consuming waste-fed fish.

Guidelines exist for the use of wastewater in fish culture (Mara and Cairncross, 1989) but are considered to be too conservative and overly restrictive. What is important is not the presence of pathogens in the farming environment but their ability to actually cause human disease. Guidelines should be based on epidemiology and not solely on presence of micro-organisms (Blumenthal et al., 1991; Blumenthal et al., 1996).

An understanding of the main risk factors and how to reduce them is therefore essential for developing best management practice. Moreover, in order to obtain a holistic view of risk, any comparison of public health and aquaculture produce derived from livestock waste-fed systems should be compared to those from other production systems. On a broader level, the risks associated with disposal of untreated livestock waste in fish ponds should be compared with alternative uses that may present greater risks to public health in developing countries. Fundamentally a fish pond is a treatment system for pathogens present in organic wastes; large diurnal variations in temperature, pH and dissolved oxygen in shallow tropical fish ponds tend to cause rapid attenuation of pathogens (Somnasang et al., 1990) (Figure 22).

6.1.2 BACTERIA AND VIRUSES

Livestock faecal wastes used as inputs into fish culture contain varying quantities of bacteria and viruses that depend on the health status of the stock and the methodology used for collection, storage and use.

Identifying hazards, assessing risks

All livestock faecal wastes must be assumed to contain pathogens. Most disease is believed to be transferred via faeces at slaughter. However, there is variation in the risk to human health based on livestock type, diet and their management. Human disease caused by many pathogens carried by livestock is difficult to diagnose. Typically, little is known about the transferability of such pathogens to humans via fish.

FIGURE 22

Rates of faecal coliform (grey-green) and bacteriophage (blue) die-off in septage-loaded fish ponds

Source: Edwards et al. (1984)

It should be assumed that all water used in aquaculture is potentially contaminated with pathogens, whether or not livestock wastes are used. Studies on warmwater fishponds at AIT showed that faecal coliforms, Salmonella and bacteriophage (used as an indicator of viruses) were sometimes present before input of wastes, suggesting that surface water is often contaminated (Edwards et al., 1983; AIT, 1986). Microbial levels increased with loading level for buffalo manure added to the ponds daily, but not for the wastes from egglaying ducks raised over the pond. In both cases, the concentration of the different microorganisms increased in the water during the early part of the experiment before falling to a constant level thereafter.

The original concentrations of microorganisms in the manure from concentrate-fed ducks were much higher than in the manure of buffalo fed a poor quality diet but phytoplankton densities were also far higher in duck manure-fed ponds.

Whilst the levels of micro-organism in manure or pond water are important in understanding risks to the producer, the level of pathogens contained in the fish at harvest is of key importance in determining risk to those preparing and consuming the fish. Levels of microorganisms found in the digestive tract of fish are much higher than in the water illustrating a likely route to infection is via contamination of hands and surfaces during preparation and cooking of fish. Buras (1990) developed the concept of threshold concentration, defined as the total number of bacteria in the fish from inspection of blood, kidney, liver, spleen, bile and digestive tract that causes appearance in the muscle. This was developed after exposing various species of fish to different levels of microorganism in the water and then determining the levels present in various parts of the fish. Above a critical level, the immune system of the fish cannot cope with bacteria levels in the water, leading to their presence in various organs and, finally, muscle. Buras (1990) found that aggregate levels of total bacteria present of between 1.0-2.0 x 10⁴ (Standard Plate Count, SPC) to be the threshold concentration for common carp. The concentration of bacteria in water that is required to reach these threshold values (critical concentration) varies between 1.0 and 5.0 x 10⁴/ml, which would require loadings far in excess of that required for optimal fish growth.

At loading rates of manure investigated in the AIT trials which maintained good water quality and led to optimal fish yields, the threshold concentrations were clearly not exceeded as the indicator micro-organisms were rarely found in organs and were never found in muscle. Salmonella are commonly found in surface waters in nature, with contamination from wild birds a likely source. However, conditions are such in waste-fed ponds that even heavier microbial loads from introduction of livestock manure are rapidly attenuated. Salmonella has also been found in shrimp pond sediment and shrimp throughout Southeast Asia however, and the cause attributed to the use of large amounts of fresh chicken manure and supplementary feeds (Reilly and Twiddy, 1992).

In contrast to bacteria, indicators for pathogenic viruses, such as bacteriophage give a measure of faecal contamination rather than the presence of pathogens. It is thought that enteric viruses are also rapidly attenuated in waste-fed ponds but their low infective dose suggest that serious attention be given to their persistence in fish ponds.

Reducing risks

Risks of passive transfer of pathogens through handling of live fish during production, harvest and processing can be reduced if physical exposure is minimized through use of appropriate clothing, especially gloves. Attention to minimise the risk of cross-contamination during processing should be avoided, as the digestive tract is the major source of pathogens. Depuration, the holding of fish in clean water without feeding, facilitates this task by reducing the amount of digestive tract contents.

Consumption of raw, certain types of processed, or undercooked fish should be avoided. Removal of visera and major organs, in addition to the digestive tract, prior to marketing ‘whole fish’ would also reduce risk.

Pre-treatment or processing of livestock waste prior to its use as a fishpond fertilizer or feed ingredient also reduces risks associated with transfer of pathogens. A comprehensive study of shrimp farms in Southern Thailand found no evidence of Salmonella (Dalsgaard et al., 1995). A critical factor for the survival of Salmonella appears to be adequate moisture. In a subsequent analysis, Salmonella was not found in chicken manure samples used in shrimp farms, as they tended to be sun-dried or dry pelletized (Dalsgaard and Olsen, 1995).

Depuration may not always be an effective method to remove micro-organisms from fish. Buras (1990) found that when common carp was cultured in heavily polluted water, depuration in clean water for a six week period was ineffective because the micro-organisms had already entered the muscle tissue. The process was more effective with tilapia raised in optimal growth conditions in wastewater-fed ponds as they contained initially lower concentrations of bacteria, with none present in organs or muscle.

Streptococcus sp. infections of fish are a relatively newly identified threat to humans. Increasingly found in cultured tilapias, S. iniae and other Streptococci that infect fish may also infect humans. Infections have been contracted when people market live fish, or consumers are cut or spined during handling or preparation of the fish. The disease appears most prevalent in intensive tilapia production systems, in which water quality is marginal and/or there is environmental stress or trauma to the fish (Plumb, 1997). It has not yet been associated with fish from integrated culture systems.

6.1.3 PARASITES

A variety of parasites (Trematodes, Nematodes, Cestodes) may be transfered through livestock waste to aquatic plants and animals (fish, amphibia, molluscs or aquatic vegetables) and then back to humans. A list of species known to be carried by fish that affect humans is given in Table 6.1.

An understanding of current systems and the potential reduction or increase in risk through integration is required. The exposure of livestock to parasites, through foraging on human faeces is often a critical part of the life cycle in lesser developed countries lacking adequate sanitation but if animals are penned, risks are minimal. The risks of promoting integration of pigs and fish among groups in which pigs are allowed to forage on human waste may, in contrast, be important. (Box 6.B)

Certain feeding practices may appear to increase the risks of infection of livestock integrated with fish production. Water plants that can be harvested opportunistically in waste water drains or raised purposefully in water contaminated with human faecal matter for livestock feed are often accompanied by attached molluscs and other invertebrates which are commonly intermediate hosts of important parasites. Increased rates of infection are unlikely via this route, however, as livestock are normally infected by a different stage of the parasite found in the faeces of humans. The integration of backyard pigs raised partly on uncooked water plants was implicated in the former widespread occurrence of Fasciolopsis buski in Central Thailand however. In some cases household pets can be reservoir hosts (e.g. Clonorchis and Opisthorchis).

TABLE 6.1

Main types of parasites. Source: Modified from Edwards (1992) and WHO (1999)

Source: AIT (1986)

In Southeast Asia where helminth-related health issues are most important, aquaculture typically develops from more extensive, and often community-based, aquatic resource management. Stocked and wild fish are often present in the same systems and thus risks associated with greater infection with Opisthorchis, which is present only in indigenous cyprinids (WHO, 1999), could be magnified by promoting integrated aquaculture.

Reducing risks

Improved sanitation or human waste disposal is a key element in the control of parasites, as is the control of pond-side vegetation that provides cover for snails which are often intermediate hosts. Education and the availability of anti-helminth drugs are also prerequisites for successful improvement of public health at the community level.

Aquaculture may also reduce the health impacts of parasite diseases. Key aspects of this are through habitat modification and host control.

Although most fish species have been found to be relatively ineffective at biological control of snail intermediate hosts (McCullough, 1990), snail-eating black carp (Mylopharyngodon piceus), and ducks can be managed to control them to a limited extent. The Louisiana red swamp crayfish (Proambarus clarkii) is being used in an attempt to control freshwater snails in Kenya (Hofkin et al., 1991). Abandoned or poorly managed fish ponds have been associated with schistosomasis in Africa (McCullough, 1990) but well managed, productive systems in which aquatic weeds and molluscs are removed or managed are probably less of a problem.

6.1.4 INSECT-VECTOR BORNE DISEASES

Poorly-managed fish ponds often become mosquito-breeding sites (Birley and Lock, 1998). Removal of surface and emergent vegetation, as a part of intensified aquaculture, reduces shelter for mosquito larvae. Introduction of aquaculture has actually decreased the incidence of disease through reduction of the habitats of the vectors or intermediate hosts such as mosquitoes and snails in Israel and China respectively.

6.1.5 INFLUENZA PANDEMICS

A major issue regarding the promotion of integrated livestock-fish production has been the possible connection between such practices and the emergence of influenza pandemics, a link which has led to heated debate in both the scientific and popular literature (Scholtissek and Naylor, 1988; Edwards et al., 1988; Edwards, 1991; Skladany, 1996). It has been claimed that the farming of pigs, poultry and fish together on the same farm is predisposing Asia, and the world, to the emergence of new virulent strains of influenza virus. Human influenza viruses are similar to poultry viruses but require change before they can infect humans, a change that can occur in pigs or between chickens and ducks (Li et al., 2003). Recent evidence suggests that not all human flu pandemics started in Asia, nor are they related to avian viruses. The outbreak of Spanish flu, which killed 20 million people in 1918-19, is believed to have started in the US, and recent analysis shows that the strain is unrelated to poultry and closer to a pig virus (Taubenberger et al., 1997).

The known possible transfer of such viruses from poultry to pigs, which act as ‘mixing vessels’ for the virus to undergo ‘antigenic shift’ is not questioned by aquaculturists, but rather the role of aquaculture in the process. Modern, integrated systems in which both poultry and pigs are raised together on the same farm with fish, are rare for fundamental economic reasons, whereas traditional farming of poultry and pigs together on farms without fish is common throughout the developing world, and especially in China. Home to many of the world’s poultry and pigs, China is also the putative origin of new strains of influenza. Where markets and production systems are intermediate between backyard and commercial, many ‘hybrid’ systems do exist however. A recent study in the environs of Ho Chi Minh City found that although pig/ fish, chicken/fish and duck/fish systems comprised over 70 percent of livestock-fish systems, over 20 percent of farms with livestock and fish raised both poultry and pigs together (Nguyen and Trinh, 1998).

Farms which raise two types of livestock together on the same farm with fish are rare. This farm is using the roof area of a pig unit to shade caged egg chickens. Casual mixing of pigs and poultry is more likely in traditional systems, irrespective of whether fish are cultured

Village chickens scavenging for waste feed within intensive battery egg units may spread disease

6.2 Chemical Hazards and Associated Risks

A major issue is how integrating livestock and fish together can reduce the level of chemical hazards and associated risks compared to stand-alone enterprises. We first explain the range of chemical hazards with a tabulated assessment of their importance to both integrated and non-integrated aquaculture compared to, where appropriate, reference to wild stocks (Table 6.2). Generally, hazards associated with intensive aquaculture, particularly of carnivorous fish, are likely to be greater than less intensive culture of herbivorous and omnivorous species because of the greater likelihood of bioaccumulation and exposure through the higher levels of water exchange required. Wild fish in unmanaged aquatic systems may suffer more from the effects of chemicals than cultured stocks as aquatic habitats often serve to drain effluents and run-off from agriculture, and complex natural ecologies are more likely to be disturbed than closely monitored culture systems. Chemicals may accumulate more in slow-growing, carnivorous species than well-fed, short-lived farmed fish.

Exposure to chemicals can be accidental or purposeful. Contamination of the surrounding environment, water or feed source for fish or livestock integrated with fish can be either acute or chronic in nature. Chemicals are also often used as part of disease control, general husbandry or as feed additives. The tendency in integrated systems is for the fish culture component to be semi-intensive i.e. relatively low densities of fish feeding low in the food chain and these are less likely to require treatment for disease, intensive disinfection or specialized feed additives. Clearly, chemical hazards inherent in livestock production have greater potential for affecting fish in such systems than vice versa.

Range of chemical hazards

Chemical hazards may arise from the use of agrochemicals, chemotheropeutants, metals, feed ingredients and organic pollutants. Agrochemicals i.e. chemical fertilizers, water treatment compounds, pesticides and disinfectants are widely used in both commercial and smallholder food production. Chemotherapeutants include a range of compounds used to control the impact of disease on both livestock and fish i.e. antimicrobials, parasiticides and hormones. The issue of bacterial resistance induced through prophylactic use of antimicrobials and drug residues that risk human health are of key interest. Exposure to metals, in addition to that from chronic or acute pollution of aquatic systems, may occur due to their use as anti-foulants and molluscides or through their inclusion as growth promoters in livestock diets. Other feed ingredients have come under recent scrutiny and, especially as use of manures as fishponds inputs may increase the pathways through which these compounds can enter the human diet, should be considered. Aquatic systems are particularly sensitive to organic pollution. In this regard exposure to chlorinated hydrocarbons that are persistent and can bioaccumulate, is of special significance (WHO, 1999).

Integrated management of livestock waste and fish production ideally leads to good practice that reduces the necessity for use of chemicals to control pests and maintain optimal conditions. The frequent collection and use of manure for fish culture can reduce problems associated with its accumulation and storage such as the spread of flying insect-born diseases or ammonia-related respiratory problems. Moreover, many farmers have found that siting of livestock pens over ponds improves the environment for the livestock through evaporative cooling; this is particularly important in the tropics where more expensive methods of controlling heat losses are uneconomic and heat stress is a major factor predisposing livestock to disease. In the sub-tropics prevention of wind-chill is often required during seasonally cooler weather.

Inland carp farms as examples of semi-intensive aquaculture often integrated with livestock production were found to have negligible use of antimicrobials (ICLARM, 1996; NACA, 1997). This is undoubtedly related to the excellent water quality and nutrition that can be maintained in semi-intensive systems, reducing the need for such inputs. The only chemicals likely to be used directly in greater quantities in semi-intensive than intensive aquaculture are chemical fertilizers, for which livestock waste often substitutes in integrated systems. However, since fish culture is typically integrated with intensive feedlot-based production, the transfer and hazards associated with chemicals present in the resultant wastes are an issue.

Antimicrobial resistance

The potential problem of bacterial strains becoming resistant to the use of antimicrobials has been raised, although rarely objectively assessed (WHO, 1999). There are two major risks of resistant strains being a hazard to human health: those associated with transmission of resistant strains from aquaculture to humans; and the possibility of non-pathogenic bacteria containing antimicrobial resistance genes being transferred to human pathogens. In the tropics, fish pathogens such Aeromonas hydophila and Edwardsiella spp. can cause human disease and the first risk, although not quantified, does exist. The second does have a potential link, particularly if drinking water is obtained from fish ponds. The risk was judged to be small as antimicrobial compounds are used to a very limited extent directly in freshwater aquaculture (WHO, 1999). However, this risk assessment disregards the large quantities of anti-microbials used both prophylatically and for disease treatment mixed with feed and water in feedlot livestock. Considerable quantities of feed and drinking water are known to be lost directly to the fish system, and the risk of survival and transfer of resistant bacteria within tropical fish ponds is a recent focus of enquiry. Although farming integrated fish has been found to increase prevalence of antimicrobial resistant bacteria in fish ponds and guts (Petersen, 2003), this is likely to be greatly outweighed by other causes of antibiotic abuse within livestock production per se and in human medicine (A. Dalsgaard, pers. comm.).

Bioaccumulation

The risk of accumulation of both drug residues and heavy metals in tissues of fish raised in semi-intensive systems is probably lower than fish raised intensively because direct use of feed additives and chemotheropeutants is very limited (WHO, 1999). Moreover, as water exchange is minimal in such systems, the likelihood of acute impacts from pollution incidences is also likely to be lower than for intensive systems using more water. Organic pollutants, however, may potentially concentrate in rainfed fish ponds within watersheds receiving runoff from agricultural land in which insecticides are used, but limited data are available. It is expected, however, that pond sediments, especially in fertilized ponds, act as a sink for these compounds, reducing losses to the wider environment with consequent effects on natural systems.

As toxins concentrate through the food chain and their growth is relatively slower, wild, carnivorous fish are more likely to accumulate metals and organic pollutants than fast-growing, cultured fish.

6.3 Biological Hazards

Micro-algae and detrital bacteria that serve as food for cultured finfish and crustaceans produce most toxic compounds affecting aquaculture. The toxins produced by blue-green algae (cyanobacteria), microcystins, are particularly potent and widespread in fertilized freshwaters (Codd, 1995; Codd et al., 1999). The optimal environments for raising filter feeding Nile tilapia are known to be highly fertile water dominated by cyanobacteria such as Microcystis aeruginosa (Colman and Edwards, 1987). The evidence suggests that not all strains of cyanobacteria are toxic and that filter feeding fish avoid ingesting toxic cells (Beveridge et al., 1993; Keshavanath et al., 1994). When fish losses occur, often at the end of plankton blooms, it is unclear if mortalities are related to the depleted levels of DO levels that occur or the toxic effects of free microcystins released into the water. However, accumulation of microcystins has been demonstrated in the livers of freshwater fish under such conditions (Codd and Bell, 1995). It has been concluded that the risk to human health through eating farmed finfish and crustacea containing these toxins is very small (WHO, 1999).

Indirect effects of aquaculture, especially in systems based on controlled fertilization, should consider the known effects of microcystins on livestock. The potential for contamination of livestock and human drinking water through nearby aquaculture does not appear to have been researched. The relative value of surface water as a potable source compared to alternative sources, and the potential contamination of ground water through seepage of microcystin-rich pond water, need to be better understood.

TABLE 6.2

Chemical hazards and associated risks to fish production

Source: Modified from WHO (1999)

A major issue is whether algal bloom problems, and health impacts on people, are more or less likely to occur in fish culture systems integrated with livestock waste than either intensive, stand alone aquaculture or infertile extensive systems. Intensive fish culture based on complete feeds can also cause rapid and sustained eutrophication. Clearly, promotion of waste-fed aquaculture requires consideration of the overall water needs of households.

6.4 Summary

The use of human and livestock waste in semi-intensive fish culture, subject to certain safeguards, can generally be considered positive in any holistic assessment of risk (Edwards, 1993). Semi-intensive systems fertilized within the carrying capacity of the system are healthy environments for fish. The fish production unit can act to ‘treat’ wastes that themselves may contain pathogens, provided certain precautionary steps are observed. Moreover, non-integrated intensive livestock and fish production carries its own risks to public health, which should be considered in any balanced comparison.