cooked infected fish can cause clonorchiasis and opistorchiasis (McGarry,. 1977). With the construction of irrigation canals for rice production, and the cultivation ...
Biological Wastes 31 (1990) 69-83
A Review of Public Health Problems Associated with the Integration of Animal Husbandry and Aquaculture, with Emphasis on Southeast Asia Ludwig C. A. Naegel Fanning Systemsand Soil ResourcesInstitute (FSSRI), University of The Philippines at Los Bafios(UPLB), College, Laguna-3720, The Philippines (Received 23 February 1989; revised version received20 April 1989; accepted 16 May 1989)
ABSTRACT Although the recycling of excrements in integrated agriculture-aquaculture farming systems offers many advantages, the spread of diseases to man via aquatic organisms multiplying in excreta-laden water needs special attention. There is strong evidence that aquatic organisms may be more important vectors for human diseases than generally realized. However, conclusive epidemiological studies linking the use of excreta in aquaculture with human diseases are lacking.
INTRODUCTION In Southeast Asia aquaculture systems are popular; with the integration of animal husbandry into such systems, a relatively new dimension on fish production has emerged. This is in the field of public health. Aquaculture, the production of aquatic organisms under controlled conditions, and the methods of introducing organic wastes and excreta from agricultural and human sources into pond systems, originated from China. The use of organic wastes and excreta for aquaculture provides to the pond system a free supply of organic fertilizer. Otherwise useless, waste products are recycled into valuable fish feed; at the same time the environment 69 Biological Wastes 0269-7483/90/$03'50 © 1990 Elsevier SciencePublishers Ltd, England. Printed in Great Britain
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receives less pollutants; and by including a biogas digester into the integrated system, it is possible to obtain additional energy from wastes. In China there is no such thing as waste--waste is only a misplaced resource which can become valuable for another product (FAO, 1977; Taiganides, 1978). Edwards (1985a) states that 'without excreta recycling, the Chinese might not be able to maintain their agriculture production'. In January 1978, the first international conference on the integration of fish farming and waste disposal took place in London and more than 80 scientists participated (Pastakia, 1978). Reviews were published by Wohlfarth and Schroeder (1979), and by Edwards (1980) about the recycling of organic wastes into fish. The Asian experiences with the integrated croplivestock fish farming systems were discussed in detail in May 1980 in Taipei, Taiwan (FFTC, 1980), and on a larger regional basis in August 1980 at the ICLARM-SEARCA Conference in Manila (Pullin & Shehadeh, 1980). Since then, a large number of publications on this topic has appeared: for example, literature about the integration of pig and fish farming (Edwards, 1985b; Tamse et al., 1985), about the utilization of duck and poultry droppings in fish farming (Barash et al., 1982; Edwards et al., 1983; Plavnik et al., 1983), about the use of cow manure in fish production (Degani et al., 1984), and even on the use of rabbit droppings for biogas and fish production (Mahadevaswamy & Venkataraman, 1988). The main reason for adding animal manures to fish ponds is to provide degradable organic matter, which is the most important component to promote the growth of bacteria and zooplankton. During the decomposition of the bacteria, CO2, phosphorus, nitrogen and other nutrients are liberated to form essential constituents for phytoplankton and algal growth (Schroeder, 1980). Phyto- and zooplankton form the base of the food chain for fish and other aquatic organisms. A part of the added excreta can also serve as direct feed for several cultivated fish species like tilapia, mullet and carp. In view of the rising costs worldwide for chemical fertilizers and for supplemental feed for aquaculture, the use of excreta from domestic animals and also from man is gaining more and more importance for the fertilization of ponds. This is especially true in tropical countries, where several important fish species are cultured, which are primary consumers and low in the food chain, like tilapia, Chinese carp species, the common carp, the milkfish (Chanos chanos) and mullet (Mugil spp.). However, the use of excreta from domestic animals and from man has two sides. On one hand, excreta provide an inexpensive source of nutrients to promote zoo- and phytoplankton growth. On the other hand, manures contain a wide variety of bacterial, viral, protozoal and helminth pathogens which may be transmitted via aquatic organisms to man and thus present a
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public health hazard. Where excreta are used in aquaculture, three groups of people may be at a risk of infection: (a)
Persons who consume raw or insufficiently cooked aquatic organisms. Adding lemon juice, garlic and onions to raw, infected fish does not destroy pathogens, contrary to c o m m o n belief. The same is true with pickling or fermenting raw fish. (b) Persons who consume raw or inadequately cooked meat of animals that have been fed with raw, infected fish or contaminated plants. (c) Persons with occupational exposure to ponds laden with excreta, and people handling and preparing contaminated aquatic products.
Reichenbach-Klinke and Elkan (1965) briefly discussed the possibility of fish as carriers of organisms that can cause human disease, and the public health aspects related to warm water pond aquaculture causing consumer and non-consumer-related diseases were considered by Brock (1983). In a study on the health constraints from integrated animal-fish farming in the Philippines, several examples were described; however, this was mainly from a taxonomic point of view (Velasquez, 1980). The degree of risk of infection varies considerably with the type of pathogen, and before an outbreak of an illness can manifest, a chain of events must occur. Whether or not an infective dose of pathogen reaches a human depends on the following: (a)
The concentration of pathogens in the manure, the time between the excretion and infection, the die-off rate of the pathogen in the new environment and the ability to multiply there. (b) Many pathogens require one or even two intermediate hosts before becoming a threat for man. (c) The practices of food handling and preparation, level of sanitation, and food consumption habits all have a significant influence on the risk of infection from diseases. (d) The pattern of human immunity determines finally whether or not an outbreak of illness occurs. Alternative routes of transmission of the pathogen have to be considered, which further obscure the steps between the presence of pathogens in excreta and the determinable human infection attributable to the introduction of excreta in aquaculture (Blum & Feachem, 1985). This rather complex situation is one reason why until today only a very limited number of epidemiological studies have focused attention on the public health risks associated with the introduction of excreta in aquaculture. It is important to point out that enormous differences of opinion exist between epidemiologists and aquaculturists. The epidemiologists treat
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animal wastes as a reservoir o f pathogenic organisms dangerous to animals and/or man. The aquaculturists, in contrast, know that in nature inter- and mono-species coprophagy always exists, that aquatic organisms are always in close contact with their own excrements, and that the conventional fish feeds are not always free of pathogens (Mueller, 1980). Additionally, in the large number of scientific studies which deal with the recycling of excreta for fish farming, only healthy animals have been used. For this reason, it is not surprising that in these studies no threat to the health of man by the use of excreta in aquaculture could be found. On the other hand, there is a lack of studies which deal with the excreta from animals raised by poor farmers who often cannot affort the prevention and control of infectious and parasitic diseases in their animals.
I M P O R T A N T P A T H O G E N S ASSOCIATED WITH T H E O U T B R E A K OF DISEASES D U E TO T H E I N T R O D U C T I O N OF E X C R E T A IN A Q U A C U L T U R E SYSTEMS In the following pages are described the most important pathogens which can be linked to public health problems caused by the introduction of excreta in aquaculture. These diseases are endemic not only in Southeast Asia, but also in many other tropical countries. However, the prevalence patterns vary across regions and continents, between rural and urban areas, and with climatic zones. Aquacultural practices, eating habits, cultural norms, and social environments are important factors determining the prevalence pattern and rendering particular diseases typical of a given community or area (Cross, 1985). In this review, the focus is on The Philippines situation; however, studies from other countries are included where relevant to the topic. After excretion and release into the external environment, eventually all pathogens will die or lose infectivity. In general, the reduction of viable pathogens is exponential, i.e. there is a rapid decrease in the numbers in the first few hours or days after excretion, with a reduced number surviving over an extended period. Variations of this die-off pattern are found in a few bacteria (e.g. Salmonella) which may temporarily multiply outside the host, and with helminths which have one or more non-infective intermediate development stages with typical die-offpatterns. A further variation is found with trematodes, which have a multiplication phase in intermediate hosts (Cross et al., 1985). Environmental factors like temperature, moisture content, nutrients, sunlight, predators and competition by other microorganisms determine the actual die-off rate and the number of organisms surviving within a given time period (Strauss, 1985).
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Enteric bacteria and viruses In the following table are listed the most important infectious microbial and protozoal pathogens with a potential for spread of diseases by the introduction of excreta in aquaculture (Table 1). From this table, it becomes very clear that the most frequent illness is diarrhoea, and that no intermediate host is involved during transmission. It is generally accepted that human and warm-blooded animal bacterial and viral pathogens do not cause acute diseases in aquatic organisms. Aquatic organisms can be considered passive carriers and mechanical transmitters of pathogens to man without the involvement of an intermediate host (Janssen, 1970). Fish grown in excreta-laden ponds carry these pathogens only passively in their intestines, gills and in the mucus of their skin. Tissue and blood from infected fish have appeared to be sterile (Nupen, 1983; Cloete et al., 1984). In recent studies, however, it has been proven that after exceeding a rather clearly defined threshold concentration of pathogens in the water, both viruses and bacteria are able to penetrate into the peritoneal fluid and even into the muscles of fish (Buras et aL, 1985; Buras et al., 1986; Buras et aL, 1987). This has an impact on the transmission of viruses and bacteria to persons who have direct contact with the intraperitoneal fluid and blood of infected fish, like fishhandlers and housewives when they are cutting, gutting and cleaning fish in preparation TABLE 1 Important Infectious Pathogens with Potential for Spread by the use of Excreta in Aquaculture (after Blum & Feachem, 1985) Pathogens
Viruses Enteroviruses Hepatitis A Rotavirus
Diseases
Intermediate host
Poliomyelitis, meningitis, fever, diarrhoea Infectious hepatitis Diarrhoea
None None None
Diarrhoea, vomiting Diarrhoea, dysentery Diarrhoea, dysentery Typhoid fever Diarrhoea, dysentery Cholera, diarrhoea
None None None None None None
Diarrhoea, dysentery Diarrhoea
None None
Bacteria Campylobacter jejuni
Path. E. coli Salmonella spp. Salmonella typhimurium Shigella spp. Vibrio cholerae
Protozoa Entamoeba histolytica Giardia lamblia
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for consumption. Viruses are immediately infective upon release into the environment and the minimal infective dose is usually low; it is believed that even a single virus may confer an infection if circumstances are suitable (Cross, 1985). Although the concentration of viruses and bacteria added with the excrements into the aquaculture system is reduced drastically by dilution, filter feeders like milkfish, mullet and tilapia can concentrate these pathogens and by this, despite the die-off pattern and high dilution in the water, can create a possible health hazard. Enteric viruses and bacteria can survive for long periods in fresh and sea water. Viable Salmonella typhimurium could be isolated from the viscera and epithelium of tilapia, and from water in pools more than 16 days after inoculation (Baker et al., 1983). Some human pathogens multiply in the gut, mucus and tissue of fishes. A marine bacterium and one of the most troublesome enteric pathogens in Japan, Vibrio parahaemolyticus, is thought to be such a pathogen (Janssen, 1970). In the Philippines, several studies have been conducted on such pathogens. Accordingly, I1. parahaemolyticus could be isolated in high numbers from milkfish (Jacalne et al., 1975). Prevalence of Salmonella in milkfish reared in brackish water ponds, was clearly associated with the fertilization of the ponds with untreated chicken manure (Manlapig, 1981). The application of untreated chicken manure to fertilize shrimp ponds significantly increased Vibrio parahaemolyticus and Salmonella in cultured shrimps, leading to problems of marketing the product to industrialized countries (Reilly et al., 1982). A study in Israel on the health risks arising from the practice of using wastewater for fish culture in ponds, and the use of water from fish ponds for agricultural irrigation, revealed a higher rate of clinical enteric diseases in villages re-using wastewater than in other villages (Fattal, 1983). In most bacterial and viral illnesses, it is very difficult to determine the exact species of pathogen without a laboratory examination, since the pathological manifestations of most enteric bacterial and viral diseases are very similar--diarrhoea. Caution, however, has to be taken in this instance. In countries like the Philippines where diarrhoea is a major health problem, the official health statistics are incomplete and do not differentiate between the microbial species of pathogens, mainly due to a lack of laboratory facilities. Therefore, the data presented have to be taken with great care. Convincing epidemiological studies have still to be carried out to link the risk of bacterial, viral or protozoal infections to consumption of aquatic organisms produced in excreta-laden ponds. Experimental studies suggest that there might be strong links between the recurrence of influenza A virus epidemics and the integration of aquaculture with duck and pig farming
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close to human dwellings. H u m a n influenza viruses can multiply in ducks, but the avian viruses are not transmitted to man. However, the transmission of genetic material from ducks to human influenza viruses appears to take place by reassortment in pigs. Pigs can become infected by and may transmit both human and avian influenza viruses not only amongst other pigs but also to the original host. Therefore, pigs seem to be 'mixing vessels' where two separate genetic reservoirs meet and where reassortment between avian and human influenza A viruses occurs, giving rise to an antigenic shift by creating new human influenza strains with new surface antigens. For this reason Scholtissek and Naylor (1988), recommend the development of integrated aquaculture systems where pigs are kept in enclosed farms separate from ducks.
Infectious protozoa It is well known that Entamoeba histolytica can be transmitted to man through the recycling of infected manure from domestic animals and from infected night-soil used as fertilizer in ponds for the production offish and of macrophytes. The live cysts can reach man or domestic animals with the consumption of contaminated plants and fresh or inadequately cooked fish. The cyst wall breaks up and trophozoites develop and invade the intestinal mucosa and other tissues of the host. Cyst formation follows with the dehydration of the fecal matter as it moves down the colon. Amoebiasis is widely distributed in countries where excreta are used as fertilizer for fish ponds. Surveys in The Philippines show a prevalence from 3 to 14% of the human population. In this country the main reason for infections with amoeba are poor sanitary disposal systems for human excreta, and inadequate provisions for safe water supplies (Institute of Public Health, UP Manila, pers. comm., 1988). The very c o m m o n use of untreated manures as fertilizer in fish ponds can add to the number of incidence of amoebiasis.
Heiminths (Trematodes) There are numerous infectious helminths which can be transmitted to man. Perhaps due to the widespread application of excreta in aquaculture systems in the Far East and in Southeast Asia, most incidences are reported from this region. This points out the need for special precautions to be taken to prevent the spread of helminth diseases with the introduction of manures in aquaculture in other regions. In this respect the often indiscriminate introduction of non-indigenous fish species without prior precautionary
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TABLE 2 Important Trematodes with a Potential for Spread by the Recycling of Excreta in Aquaculture Pathogen 1 and 2
Intermediate hosts
Final hosts
Clonorchis sinensis (Chinese liver fluke)
Freshwater snail-Cyprinidae
Man, cat, dog
Echinostoma ilocanum (Garrison's fluke)
Freshwater snail (Pila luzonica)
Man, dog, rat
Fasciola hepatica (Liver fluke)
Amphibious snail-aquatic plants
Man, pig, cattle
Heterophyes heterophyes (yon Siebold's fluke)
Freshwater snail-Mullet, tilapia, catfish
Man
Metagonimus yokogawai
Freshwater snail-Salmonids, Cyprinids
Man
Fasciolepsis buski (Intestinal fluke)
Freshwater snail-aquatic plants
Man, pig, cattle
Opisthorchis felineus
Freshwater snail Cyprinids, tilapia
Man, cat, dog, pig "
Paragonimus westermani (Oriental fluke)
Freshwater snail Crayfish, crab
Man, cat, dog, rat
Schistosoma spp.
Freshwater snail (Hepato-intestinal/ urinary schistosomiasis/ bilharziosis)
Man, cat, dog, rat goat, dog
measures o f quarantine can cause the spread of helminth diseases to new areas. The life cycle of helminths includes one or two intermediate hosts. This fact reduces the potential for transmission. If however, the appropriate host or hosts are present in the water the potential for spread increases significantly, since the larval stages o f the trematodes (flukes) multiply in the host. Transmission to man can only occur if appropriate host/hosts are present and if man consumes either raw or partially cooked flesh from the intermediate host which contains the helminthic larva. The most c o m m o n trematodes which can be transmitted through the introduction o f excreta in aquaculture, and which pose potential health hazards for man, are briefly described below (Table 2). Note the first and intermediate and the final hosts. A detailed description o f their often complex life cycles can be found in standard textbooks of parasitology.
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Eggs of Clonorchis sinensis (Chinese liver fluke), Opisthorchis viverrini and O. felineus are excreted by man, pig, cat and dog and are transmitted via freshwater snails as their first intermediate host, and via freshwater fish as their second intermediate host. The consumption of raw or insufficiently cooked infected fish can cause clonorchiasis and opistorchiasis (McGarry, 1977). With the construction of irrigation canals for rice production, and the cultivation of tilapia in excreta-laden water, the incidences of opisthorchiasis have reached an alarming dimension in Thailand. This is attributable to the consumption of raw tilapia infected with O. viverrini. In man the eggs of O. viverrini are not excreted but they are responsible for painful immune reactions, which can eventually lead to liver cirrhosis and death (Merkle, A., GTZ, Eschborn, FRG, pers. comm., 1986). In the northern parts of the Philippines, infections with the intestinal fluke Echinostoma ilocanum (Garrison's fluke) are common. In endemic areas about 5% of the population suffer from this parasite. The infection can be traced to the consumption of raw or inadequately cooked freshwater snails grown in excreta-laden ponds. In some parts of the country, freshwater snails are considered to be a delicacy. Feeding aquatic macrophytes, which are contaminated with infected snails, to hogs and cattle and the recycling of their manure in ponds increases the incidence of infection with Garrisons's fluke. In Asia the c o m m o n trematodes affecting man, pig and cattle are Fasciola hepatica, the cattle or sheep liver fluke, and Fasciolepsis buski (giant intestinal fluke). These are transmitted by the use of infected manures of cattle, sheep and man, as fertilizer for fish ponds, via freshwater snails as their first intermediate host and the consumption of raw or inadequately cooked aquatic vegetation. Encysted and developed metacercaria of the trematodes are found on the roots, on the fruits and leaves of macrophytes, like the water chestnut (Eliocharis tuberosa), water spinach (Ipomoea reptans) or the water caltrop (Tropa bicornis). With the consumption of the raw or uncooked infected plants, the metacercaria hatch in the d u o d e n u m of the final host. In the Philippines the incidence of human infection with Fasciola spp. and Fasciolepsis spp. is low, since all aquatic plants for human consumption are normally well-cooked; however, most water buffalos are infected and present an important reservoir for this fluke disease. The consumption of raw mullet, tilapia, milkfish, or catfish (Clarius batrachus) can cause infections with Heterophyes heterophyes (von Siebold's fluke), and the consumption of raw freshwater salmonids and cyprinids are responsible for infections with Metagonimus yokagawai. Freshwater snails serve as the first intermediate host of these two species of flukes
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(Reichenback-Klinke et al., 1965). In the southern part of The Philippines, infections with the Oriental lung fluke (Paragonimus wastermani) are common. When rice fields for integrated rice-fish production are fertilized with infected human excrements, carnivorous animals or pigs, the eggs of the fluke can find their first intermediate host in a freshwater snail (Brotia asperata). The developed cercaria find their second host in a freshwater crab (Sundathelphusaphilippina) where they encyst as metacercaria. Infection can then easily follow, since crabs and crayfish grilled at open fires during parties and only partly cooked meat sucked out from the shell are considered in the Philippines as delicacies. Once in the human host, the worms hatch in the duodenum and the young flukes penetrate the intestinal wall and finally enter the lungs. Although the eggs of the lung flukes are coughed up with the sputum, and in most cases are expectorated, they are also sometimes swallowed. Swallowed eggs are found in the feces of man and pig, and through the recycling of these infested excrements in aquaculture, another life cycle of the lung fluke can start again. All the above-described trematodes can only be transmitted to man and other warm-blooded animals by the consumption of raw or insufficiently cooked fish, crabs, or aquatic plants. However, the transmission of the Schistosoma trematodes (Schistosomajaponicum or blood fluke, S. mansoni or hepato-intestinal fluke, S. haematobium Bilharziose or urinary fluke) is an occupational risk for persons working in ponds fertilized with untreated infected excreta. Eggs of the Schistosoma fluke are transmitted with the excreta of man and/or domestic animals to a freshwater snail. The infective cercaria swim in the water until they come in contact with man or domestic animals. They penetrate the skin and enter the circulatory system where they become adults in 24 h and start to lay eggs. Not only man is infected by Schistosoma, but also cattle, dogs and even goats, when coming into contact with infested water. In The Philippines alone about 700000 people are suffering from schistosomiasis (S. japonicum), mainly the aquaculture workers and rice field farmers. The use of infected excrements of domestic animals for fertilizing the fish ponds is one of the suspected basic causes. To control schistosomiasis, a number of measures has to be implemented. There should be avoidance of the introduction of infected excreta in aquaculture; there should be snail control by biological means, for example through the introduction of snail-eating fish species, and control through chemical and water management techniques (De Bont & de Bont Hers, 1952; Michelson, 1957; Malek, 1984). The giant Malaysian prawn, Macrobrachium rosenbergii, is a predator for schistosome vector snails in fish ponds and can act in this way as a biological control for the spread of schistosomiasis in aquaculture (Lee et al., 1982).
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CONCLUSIONS In Southeast Asia, as in other regions, the integration of animal husbandry and the recycling of animal manures as a nutrient source in aquaculture offer many benefits. However, because of the widespread use of untreated excreta, the spread of a large number of viral, bacterial, protozoal and helminthic diseases may be compounding public health problems. Special attention has to be directed to the health aspects to avoid the spread of diseases. There are several methods of minimizing the health hazards:
1. The use of pathogen-free excreta. Unfortunately, complete destruction of pathogens through the methods of waste treatment before applying excreta to fish ponds is, from economic and technical points of view, not easy to achieve, the anaerobic treatment of excreta in biogas digesters, often thought to result in a pathogen-free effluent, today seems to be insufficient to decrease the concentration of pathogens to safe levels, due to the too-short detention time in the digesters (Feachem et al., 1981). The only process that can produce a largely pathogen-free material is aerobic composting, a method widely applied in China (Edwards, 1985a). 2. Control of spread of pathogens through veterinary activities and through health education. To reduce the risk of infections through the recycling of manures from domestic animals, special care has to be directed to the health of the animals to prevent them from becoming a reservoir for human pathogens. Recycling of manures from healthy animals is leading to aquatic products free from microbial pathogens and human parasites (Hopkins & Cruz, 1982; Rice et aL, 1984). Through public health education, preventive medicine and medical treatment of illnesses, the spread of infections can be reduced. 3. Pond management. The clearing of vegetation from pond banks can help to control snails, which are the intermediate hosts for many pathogenic helminths, expecially Clonorchis and Schistosoma. 4. Lengthening of the food chain. Although the use of untreated manures and night-soil is a common practice, excrements should be added to aquaculture systems with prior storage for at least two weeks to destroy the eggs of trematodes. If possible, the aquatic product should not be used for human consumption, but processed and used as animal feed. The lengthening of the food chain can be considered as an additional safeguard to public health. This is important in view of the fact that many fish species tend to consume excreta directly and by this might accumulate and incorporate bacterial and viral pathogens not only in the intestines, but also in the intraperitoneal fluid and in the muscles.
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5. Depuration of aquatic organisms before harvesting. If fish and other aquatic organisms are produced for human consumption in excreta-recycle systems, then at least prior to harvesting and marketing, the organisms should be allowed to depurate for several weeks in clean water. This method is widely applied in China and Vietnam, and in view of the results with fish which show the incorporation of microbial pathogens even into muscles, depuration is a very important step to minimize possible health hazards from the use of excreta in aquaculture. 6. Handling and processing of aquatic products. The importance of good hygienic conditions should be stressed at all stages of fish handling and processing. 7. Consumption of raw aquatic products discouraged. As one of the most important possibilities to minimize the health hazards from the introduction of excreta in aquaculture systems, the consumption of raw or inadequatelycooked aquatic products should be strongly discouraged. Through the cooking of infected aquatic organisms, all pathogens can be destroyed.
ACKNOWLEDGEMENTS This work would not have been possible without the many discussions with faculty members of the Institute of Public Health, UP Manila, and without the help from many colleagues in providing me with bibliographic references. In the editing of this article, Mr Frank Hilario has been very helpful. The author thanks them all and fully appreciates their friendly cooperation. REFERENCES Baker, D. A., Smitherman, R. O. & McCaskey, T. A. (1983). Longevity of Salmonella typhimurium in Tilapia aurea and water from pools fertilized with swine waste. Applied Environmental Microbiology, 45(5) 1548-54. Barash, H., Plavnik, I. & Moav, R. (1982). Integration of duck and fishfarming: Experimental results. Aquaculture, 27, 129--40. Blum, D. & Feachem, R. G. (1985). Health aspects of nightsoil and sludge use in agriculture and aquaculture. Part III. An epidemiological perspective. IRCWD Report No. 05/85. International Reference Centre for Waste Disposal, Duebendorf, Switzerland, 86 pp. Brock, J. A. (1983). Pond production systems: Diseases, competitors, pests, predators and public health considerations. In Principles & Practices of Pond Aquaculture: A State of the Art Review, ed. J. E. Lannan, R. O. Smitherman & G. Tschobanoglous. Oregon State University, Newport, Oregon, USA. pp. 169-85.
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Buras, N., Duek, L. & Niv, S. (1985). Reactions of fish to microorganisms in wastewater. Applied Environmental Microbiology, 50(4) 989-95. Buras, N., Hepher, B., Sandbank, E., Niv, S., Duek, L., Hayes, E. & Haber, E. (1986). Pathogen transfer/wastewater (Israel). In Reclamation of Nutrients, Water and Energy from Waste, IDRC Manuscript Report 124e, Ottawa, Canada, pp. 59-72. Buras, N., Duek, L., Niv, S., Hepher, B. & Sandbank, E. (1987). Microbiological aspects of fish grown in treated wastewater. Water Research, 21(1) 1-10. Burns, R. P. & Stickney, R. R. (1980). Growth of Tilapia aurea in ponds receiving poultry wastes. Aquaculture, 20, 117-21. Cloete, T. E., Toerien, D. F. & Pieterse, A. J. H. (1984). The bacteriological quality of water and fish of a pond system for the treatment of cattle feedlot effluent. Agricultural Wastes, 9, 1-15. Cross, P. (1985). Health aspects of night soil and sludge use in agriculture and aquaculture. Part I: Existing practices and beliefs in the utilization of human excreta. IRCWD Report 04/85, pp. I/1-I/23. International Reference Centre for Waste Disposal, Duebendorf, Switzerland. Cross, P., Strauss, M., Blum, D. & Feachem, R. (1985). Health aspects of night soil and sludge use in agriculture and aquaculture. WHO International Reference Centre for Wastes Disposal News, 23, 1-10. de Bont, A. F. & de Bont Hers, M. J. (1952). Mollusc control and fish farming in Central Africa. Nature, 170, 323-4. Degani, G., Desoretz, C. & Levanon, D. (1984). The influence of cow manure on growth rates of Oreochromis aureus and Clarias lazera in Israel in outdoor tanks. Bamidgeh, 36(4) 114 20. Edwards, P. (1980). A review of recycling organic wastes into fish, with emphasis on the tropics. Aquaculture, 21(3) 261-79. Edwards, P. (1985a). Aquaculture: A component of low cost sanitation technology. World Bank Tech. Paper, 36, Washington, USA, 45 pp. Edwards, P. (1985b). Pigs over fish ponds. Pig International, 15(7) 8-10. Edwards, P., Kaewpaitoon, K., Meewan, A., Harnprasitkam, A. & Chantachaeng, C. (1983). A feasibility study offish/duck integrated farming at the family level in Central and Northeast Thailand. AIT Research Report No. 163. Asian Institute of Technology, Bangkok, Thailand, 48 pp. FAO (1977). China: Recycling of organic wastes in agriculture. FAO, Soils Bulletin, 40, Food and Agruculture Organization, Rome, Italy, 105 pp. Fattal, B. (1983). The prevalence of viral hepatitis and other enteric disease in communities utilizing wastewater in agriculture. Water Science Technology, 15, 43-58. (cited by D. Blum & R. G. Feachem 1985). Feachem, R. G., Bradley, D. J., Garelick, H. & Mara, D. D. (1981). Appropriate Technology for Water Supply and Sanitation. Health Aspects of Excreta and Sillage Management: A State-of-the-Art Review. The World Bank, Washington, USA. FFTC (1980). Integrated Crop-Livestock-Fish Farming. FFTC Book Series No. 16, Food and Fertilizer Technology Center, Taiwan, Peoples' Republic of China, 147 pp. Hojovec, J. (1977). Health effects from waste utilization. In Animal Wastes, ed. E. P. Taiganides. Science Publishers Ltd, London, UK, pp. 105-9. Hopkins, K. D. & Cruz, E. M. (1982). The ICLARM-CLSU integrated animal-fish
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