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 Systems and Soil Resources Institute (FSSRI),
University of The Philippines at Los Bafios (UPLB),
College, Laguna-3720, The Philippines
(Received 23 February 1989; revised version received 20 April 1989;
accepted 16 May 1989)
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.
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
Biological Wastes 0269-7483/90/$03'50 © 1990 Elsevier Science Publishers Ltd, England.
Printed in Great Britain
Ludwig C. A. Naegel
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 crop-
livestock 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,
1985), about the utilization of duck and poultry
droppings in fish farming (Barash
1983), about the use of cow manure in fish production (Degani
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 decompo-
sition 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
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
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
Health problems in integrated agriculture-aquaculture farming 71
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 common 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 intro-
duction 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
72 Ludwig C. A. Naegel
animal wastes as a reservoir of 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.
IMPORTANT PATHOGENS ASSOCIATED WITH THE
OUTBREAK OF DISEASES DUE TO THE INTRODUCTION OF
EXCRETA IN AQUACULTURE 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 micro-
organisms determine the actual die-off rate and the number of organisms
surviving within a given time period (Strauss, 1985).
Health problems in integrated agriculture-aquaculture farming
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
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
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
Important Infectious Pathogens with Potential for Spread by the use of Excreta in
Aquaculture (after Blum & Feachem, 1985)
Pathogens Diseases Intermediate host
fever, diarrhoea None
Infectious hepatitis None
Diarrhoea, vomiting None
Diarrhoea, dysentery None
Diarrhoea, dysentery None
Typhoid fever None
Diarrhoea, dysentery None
Cholera, diarrhoea None
Diarrhoea, dysentery None
Ludwig C. A. Naegel
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
could be isolated from the viscera and
epithelium of tilapia, and from water in pools more than 16 days after
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,
to be such a pathogen (Janssen, 1970).
In the Philippines, several studies have been conducted on such
could be isolated in high
numbers from milkfish (Jacalne
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
and Salmonella in cultured
shrimps, leading to problems of marketing the product to industrialized
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
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
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
Health problems in integrated agriculture-aquaculture farming
close to human dwellings. Human 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.
It is well known that
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 common use of
untreated manures as fertilizer in fish ponds can add to the number of
incidence of amoebiasis.
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
76 Ludwig C. A. Naegel
Important Trematodes with a Potential for Spread
Aquaculture by the Recycling of Excreta in
Pathogen 1 and 2 Intermediate hosts Final hosts
(Chinese liver fluke)
(yon Siebold's fluke)
( Pila luzonica)
Mullet, tilapia, catfish
Man, cat, dog
Man, dog, rat
Man, pig, cattle
Man, pig, cattle
Man, cat, dog, pig "
Man, cat, dog, rat
Man, cat, dog, rat
measures of quarantine can cause the spread of helminth diseases to new
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 of 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 common trematodes which can be transmitted through the
introduction of 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 of their often
complex life cycles can be found in standard textbooks of parasitology.
Health problems in integrated agriculture-aquaculture farming
(Chinese liver fluke),
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,
With the construction of irrigation canals for rice production, and the
cultivation of tilapia in excreta-laden water, the incidences of opisthor-
chiasis have reached an alarming dimension in Thailand. This is attributable
to the consumption of raw tilapia infected with O.
In man the eggs
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
(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
In Asia the common trematodes affecting man, pig and cattle are
the cattle or sheep liver fluke, and
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
or the water caltrop
With the consumption of the raw or
uncooked infected plants, the metacercaria hatch in the duodenum of the
final host. In the Philippines the incidence of human infection with
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
can cause infections with
fluke), and the consumption of raw freshwater salmonids and cyprinids are
responsible for infections with
serve as the first intermediate host of these two species of flukes
78 Ludwig, C. A. Naegel
(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).
Health problems in integrated agriculture-aquaculture farming
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
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
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.
80 Ludwig C. A. Naegel
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
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 inadequately-
cooked aquatic products should be strongly discouraged. Through the
cooking of infected aquatic organisms, all pathogens can be destroyed.
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
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.
Health problems in integrated agriculture-aquaculture farming 81
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,
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,
FFTC (1980). Integrated Crop-Livestock-Fish Farming. FFTC Book Series No. 16,
Food and Fertilizer Technology Center, Taiwan, Peoples' Republic of China,
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
82 Ludwig C. A. Naegel
farming project. Final Report. ICLARM Tech. Rep. 5, Manila, Philippines,
Jacalne, A. V., Manuson, N. M. & Bautista, S. L. (1975). Studies on Vibrio
parahaemolyticus in seafoods (shellfish, shrimps, crabs and various sp. of fish)
and coastal waters in and around Metro Manila, Rep. of the Philippines. Paper
presented at the 8th Intern. Symp. on Vibrio parahaemolyticus. Osaka, Japan.
Mimeographed, 5 pp.
Janssen, W. A. (1970). Fish as potential vectors of human bacterial diseases. In
Symposium on Diseases of Fish and Shellfishes, Washington DC, USA,
Lee, P. G., Rodrick, G. E., Sodeman, W. A. & Blake, N. J. (1982). The giant
Malaysian prawn, Macrobrachium rosenbergii, a potential predator for
controlling the spread of schistosome vector snails in fish ponds. Aquaculture,
Mahadevaswamy, M. & Venkataraman, L. V. (1988). Integrated utilization of rabbit
droppings for biogas and fish production. Biological Wastes, 25, 249-56.
Malek, E. A. (1984). Impact of fishponds on public health in Rwanda with special
reference to schistosomiasis. ICA Communicae, 7(1) 2-3.
Manlapig, E. T. (1981). A prevalence of salmonella in milkfish obtained from five
different sources. University of the Philippines, College of Fisheries, BS thesis,
McGarry, M. G. (1977). Domestic waste as an economic resource: Biogas and fish
culture. In Water, Wastes and Health in Hot Climates, ed. R. Feachem, M. G.
McGaarry & D. Mara. John Wiley & Sons, London and New York,
Michelson, E. H. (1957). Studies on the biological control of Schistosome-bearing
snails. Predators and parasites of freshwater mollusca: A review of the
literature. Parasitology, 47, 413-26.
Miieller, Z. O. (1980). Feed from animal wastes: state of knowledge. FAO, Animal
Production Health Paper, 18, Rome, 190 pp.
Nugent, C. G. (1978). Integration of the husbandry of farm animals and fish with
particular reference to pig raising in tropical areas. In Proceedings of the
Conference on Fishfarming and Wastes, 4-5 January 1978, University College
London, UK. ed. C. M. R. Pastakia. 151 pp.
Nupen, E. M. (1983). Possible health hazards in fish farming using sewage. Paper
presented at the Seminar of Appropriate Technology Transfer in Water Supply
and Sanitation. Venda, 28-30 Sept. 1983. Mimeographed, 14pp.
Pastakia, C. M. R. (ed.) (1978). Proceedings of the Conference on Fishfarming and
Wastes. 4-5 January 1978, University College, London, UK, 151 pp.
Plavnik, I., Barash, H. & Schroeder, G. 1983. Utilization of ducks' droppings in fish
farming. Nutrition Reports International, 28(3) 635-41.
Pullin, R. S. V. & Shehadeh, Z. H. (ed.) (1980). Integrated agriculture-aquaculture
farming systems. ICLARM Conference Proceedings, 4, International Center
for Living Aquatic Resources Management, Manila and Southeast Asian
Center for Graduate Study and Research in Agriculture, College, Los Bafios,
Laguna, Philippines, 258 pp.
Reichenbach-Klinke, H. & Elkan, E. (1965). Fish as carriers of human diseases. In
The Principal Diseases of Lower Vertebrates. Academic Press, London and
New York, pp. 190-4.
Health problems in integrated agriculture-aquaculture farming 83
Reilly, A., Bernarte, M. A. & Dangla, E. (1982). Microbiological problems
associated with processing cultured prawns for the export market. Philippine
Journal of Food Science and Technology, 6(1-2) 41-55.
Rice, T., Buck, D. H., Gordon, R. W. & Tazik, P. P. (1984). Microbial pathogens and
human parasites in an animal waste polyculture system. Progressive Fish
Culturist, 46(4) 230-8.
Scholtissek, C. & Naylor, E. (1988). Fish farming and influenza pandemics. Nature,
Schroeder, G. L. (1980). Fish farming in manure-loaded ponds. In ICLARM Conf.
Proc. 4, Laguna, Manila, Philippines, ed. R. S. V. Pullin & Z. H. Shehadeh.
Strauss, M. (1985). Health aspects of night-soil and sludge use in agriculture and
aquaculture. Part II: Pathogen survival. IRCWD Report No. 04/85, pp.
II/1-II/87 and A1-A7. International Reference Centre for Waste Disposal,
Taiganides, E. P. (1978). Principles and techniques of animal waste management and
utilization. In FAO, Soils Bulletin, 36, Food and Agriculture Organization,
Rome, Italy, pp. 341-62.
Tamse, A. F., Fortes, N. R., Catedrilla, L. C. & Yuseco, J. E. H. (1985). The effect of
using piggery wastes in brackishwater fishpond on fish production. University
of the Philippines at the Visayas Fisheries Journal, 1(1) 69-76.
Velasquez, C. C. (1980). Health constraints to integrated animal-fish farming in the
Philippines. In ICLARM Conf. Proc. 4, Laguna, Manila, Philippines, ed. R. S.
V. Pullin & Z. H. Sehadeh. pp. 103-111.
Wohifarth, G. W. & Schroeder, G. L. (1979). Use of manure in fish farming--A
review. Agricultural Wastes, 1,279-99.