[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]
Public, Animal, and Environmental Health Implications of Aquaculture
E. Spencer Garrett,* Carlos Lima dos Santos, and Michael L. Jahncke
*National Seafood Inspection Laboratory, Pascagoula, Mississippi, USA;
Food and Agriculture Organization of the United Nations, Rome, Italy;
Virginia Tech Seafood Research and Extension Center, Hampton, Virginia,
USA
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      Aquaculture is important to the United States and the world's
      fishery system. Both import and export markets for aquaculture
      products will expand and increase as research begins to remove
      physiologic and other animal husbandry barriers. Overfishing of
      wild stock will necessitate supplementation and replenishment
      through aquaculture. The aquaculture industry must have a
      better understanding of the impact of the "shrouded" public and
      animal health issues: technology ignorance, abuse, and neglect.
      Cross-pollination and cross-training of public health and
      aquaculture personnel in the effect of public health, animal
      health, and environmental health on aquaculture are also
      needed. Future aquaculture development programs require an
      integrated Gestalt public health approach to ensure that
      aquaculture does not cause unacceptable risks to public or
      environmental health and negate the potential economic
      and nutritional benefits of aquaculture.
U.S. Fisheries System
Coastal estuaries serve as a breeding ground and provide habitats for more
than 75% of commercial landings and 80% to 90% of the recreational catch of
fish and shellfish. From these habitats, hundreds of species of seafood are
produced. Aquacultured species now contribute up to 15% of the U.S. supply
(1,2). Wild species are harvested by 17,000,000 recreational anglers and
nearly 300,000 commercial harvesters. Commercial harvesters deploy 93,000
vessels, while recreational fishermen have millions of recreational fishing
boats. Nearly 5,000 domestic plants are located in every state throughout
the United States, not just in the coastal areas (3). Current per capita
consumption of commercially harvested species averages 15 pounds; it is
estimated that per capita consumption of recreationally harvested seafood
approaches an additional 3 to 4 pounds per person (4).
The seafood business community--in the United States and in other
industrialized countries--cannot rely solely on domestically produced stock.
For a number of years, more than half of U.S. seafood consumption has
relied on imported stock. Currently, the United States imports more than
50% of the consumed seafood, which originates in 172 countries around the
world (3). This trend toward economic reliance on imported stock has
steadily increased over the past 10 years so that now the United States is
the world's second largest importer of seafood. The principal seafood
imports are tuna, shrimp, salmon, lobster, and groundfish (3).
It is difficult to determine where imported fish was harvested. For
example, the United States imports salmon from Switzerland and Panama,
although neither Switzerland nor Panama is noted for vast salmon resources.
U.S. participation in the international seafood trade is very complex,
since in addition to being the world's second largest importer, the United
States is also the world's second largest exporter of seafood (3). This
dichotomy requires that U.S. marketing and import/export food control
inspection strategies be carefully planned. For example, the United States
exports seafood to 162 countries, which has come about with the full
development of northwest and Alaska fisheries and improved efficiency in
processing techniques. Major U.S. exports are salmon, crab, surimi, fish
blocks, groundfish, flatfish, shrimp, and lobster (3).
Current Aquaculture Status
In 1996, U.S. aquaculture production of nearly 227,000 metric tons
consisted of baitfish, catfish, salmon, trout, clams, crawfish, mussels,
oysters, fresh and saltwater shrimp, and miscellaneous species such as
ornamental fish, alligators, algae, aquatic plants, tilapia, and hybrid
striped bass. The United States exported principally rainbow trout,
Atlantic salmon, tilapia, catfish, freshwater crawfish, and live mussels to
19 countries in Europe, North and South America, and Asia. Freshwater
crawfish led the export seafood market at slightly over $8 million, with
the other species accounting for less than $1 million each (3). The United
States also imports large volumes of aquacultured products, approximately
$2.5 billion in cultured products, primarily shrimp and salmon. Imported
cultured seafood accounts for most of the current U.S. trade deficit for
edible fishery products, which was approximately $3.5 billion in 1995.
The Safety of Seafood
Most seafood is safe; however, like all foods, it carries some risk. The
food safety issues for seafood are highly focused, well-defined, and
limited to a very few species. For seafood-borne illnesses (in which the
cause was known) reported to the Centers for Disease Control and
Prevention, more than 90% of the outbreaks and 75% of the individual cases
were associated with ciguatoxin (from a few reef fish species) and
scombrotoxin (from tuna, mackerel, bluefish, and a few other species) and
the consumption of mollusks (mostly raw) (5-12).
Hazards associated with the consumption of all food (including seafood) can
be categorized into three areas: product safety; food hygiene (clean vs.
dirty plants, wholesome vs. unwholesome products); and mislabeling or
economic fraud. Traditionally, the food safety risks of seafood products
(aquacultured and wild-caught) have been subcategorized by environment,
process, distribution, and consumer-induced risk; the environmental risk
category is further subdivided into natural hazards (e.g., biotoxins) and
anthropogenic contaminants (e.g., polychlorinated biphenyls) (13).
"Shrouded" Aquaculture Hazards
The future of aquaculture is bright; aquaculture products are as safe and
wholesome as wild-caught species. However, in addition to the consumer
hazards listed above, there are some less obvious "shrouded" public health
hazards associated with ignorance, abuse, and neglect of aquaculture
technology.
Technology Ignorance
A common practice in many developing countries is the creation of numerous
small fish pond impoundments. However, this approach may have a greater
adverse effect on human health than the creation of a single large
impoundment (14). Small impoundments greatly increase the overall aggregate
shoreline of ponds, causing higher densities of mosquito larvae and
cercaria, which can increase the incidence and prevalence of diseases such
as lymphatic filariasis and schistosomiasis, respectively. Centralized
planning approaches for new freshwater and marine aquaculture sites should
include discussions of the potential effect of large or small impoundments
on such issues as disease transmission, water supply, irrigation, and power
generation (14).
Ignorance of the microbial profile of aquaculture products can also affect
human health as evidenced by the recent transmission of streptococcal
infections from tilapia to humans, which resulted in several meningitis
cases in Canadian fish processors (15). A change in marketing strategies to
sell live fish in small containers, instead of ice-packs, resulted in human
Vibrio infections from live tilapia in Israel in 1996. Such bacteria can be
present in other aquacultured and wild-caught species in addition to
tilapia.
Ignorance of the hazards associated with the use of untreated animal or
human waste in aquaculture ponds to increase production also has tremendous
human health implications (16). For centuries, food growers have cultured
species in waste-water-fed ponds and grown secondary vegetable crops in
waste water and sediment material in integrated aquaculture operations.
However, the potential for transmission of human pathogens to cultured
species and secondary vegetable crops is rarely considered by fishery
aquaculturists. For example, of more than 250 presentations at the 1997
World Aquaculture Society meeting held in Seattle, Washington, few referred
to the potential human health implications of aquaculture (17).
The potential transmission of animal pathogens from exotic aquacultured
species to wild-stock species also affects animal health. Recent outbreaks
of taura, yellow spot, and white head viruses have occurred in aquaculture
shrimp in South Carolina and Texas. Recent studies indicate that native
wild white shrimp may also be susceptible to these exotic viruses (18).
Technology Abuse
Technology abuse includes the willful misuse of therapeutic drugs,
chemicals, fertilizers, and natural fishery habitat areas. The widespread
use and misuse of antibiotics to control diseases in aquaculture species is
worldwide and will probably increase as aquaculturists move towards more
intensive animal husbandry rearing techniques and stocking densities. For
example, the illegal use of chloramphenicol in shrimp culture to control
diseases may result in violative levels in the harvested product.
Similarly, the improper or illegal use of chemicals (e.g., tributyl tin) to
control pond pests such as snails can also result in human health hazards.
The abuse and misuse of raw chicken manure as pond fertilizer may result in
the transmission of Salmonella from manure to the cultured product (16).
The destruction of mangrove areas to build aquaculture ponds can have a
drastic impact on the survival of wild aquatic species through the
degradation of essential fish habitats and nurseries. In Brazil,
destruction of mangrove areas for shrimp ponds affected climatic changes to
such an extent that the aquaculture operations have been terminated because
consequent reduced rainfall resulted in excessive pond salinity (19).
Technology Neglect
The final "shrouded" hazard associated with aquaculture involves technology
neglect, which includes such events as the abandonment of small aquaculture
ponds in tropical countries, leading to increased mosquito habitats and
concomitant increases in malaria (14). Facility management can be
responsible for technology neglect if employees are not trained in the
proper use and application of therapeutics and chemicals, for example.
Finally, from an animal health perspective, ignorance or willful neglect of
the International Council for Explorations of the Sea/European Inland
Fisheries Advisory Commission Code of Practice for the Introduction and
Transfer of Marine Organisms can result in the escape of exotic species and
animal pathogens into the environment with a potential tragic impact on
native aquatic species (20).
Health Control Considerations
Human Health
Procedures to help protect humans from aquaculture-associated risks include
better education and training of aquaculture personnel on the proper use
and storage of therapeutics and chemical compounds. Additional research on
new more effective and, we hope, safer, antibiotic and vaccine treatment of
aquaculture species is under way. Likewise, certain extralabel use
applications for selected antibiotics are under consideration. Streamlined
enforcement efforts are being developed to ensure compliance with new food
safety regulations and new regulatory control procedures such as Hazard
Analysis and Critical Control Points (HACCP) and the application of HACCP
principles to animal and environmental control procedures (21,22).
The Food and Agriculture Organization and World Health Organization
recommend that the HACCP concept be applied to fresh water aquaculture
programs to control foodborne digenetic trematode infections in humans.
Experiments are being carried out in Asia by a multidisciplinary team of
experts in public health, parasitology, aquaculture, fisheries extension,
and fish inspection (22). In one study in Vietnam, experimental activities
were conducted in two side-by-side fish ponds. In the experimental ponds,
fish were cultured in conjunction with HACCP principles, and control pond
fish were cultured according to conventional local aquaculture practices
(22). Water supply, fish fry, fish feed, and pond conditions in the
experimental pond were identified as critical control points. The HACCP
principles of hazard analysis, preventative measures, critical limits,
monitoring, recordkeeping, and verification procedures relating to the
critical control points were applied; study results showed Clonorchis
sinensis eggs and fish infected with the parasite metacercaria and the
first intermediate host (Melanoides tuberculata) in the experimental ponds
(22). Forty-five percent of control pond fish were infected with C.
sinensis metacercaria, while white fish from the experimental pond
monitored according to HACCP principles were completely free of trematode
infection (22). Preliminary results indicate that application of
HACCP-based principles to silver carp culture in North Vietnam is an
effective way to prevent and control C. sinensis. Similarly, the
application of these principles to fresh water aquaculture ponds in
Thailand and Laos to control Opisthorchis viverrini infections has also
been successful. Additional studies are recommended to confirm these
preliminary results (22).
Animal Health
Procedures to safeguard animal health are set out in the International
Council for Explorations of the Sea and the European Inland Fisheries
Advisory Commission Codes of Practice, which describe how to prevent the
adverse effects of introducing new and exotic species and emerging animal
pathogens. Education and on-site training programs for aquaculture
employees will help them understand the detrimental impact of introduction
of exotic species and animal pathogens, misuse and abuse of therapeutics
and chemicals, and willful habitat destruction. High priority issues also
include implementation of biosecurity procedures in aquaculture operations
to prevent the escape and spread of exotic species and pathogens into the
facility and surrounding natural environment and the use of the HACCP
principles to help control the spread of exotic pathogens to wild aquatic
populations (17,23).
The application of HACCP principles to control transmission of exotic
shrimp viruses from cultured to wild shrimp was proposed at a shrimp
pathogen workshop held in June 1996 in New Orleans, Louisiana (21). Natural
resource regulatory agencies are concerned about the possible transmission
of exotic shrimp pathogenic viruses, recently found in shrimp aquaculture
ponds in Texas and South Carolina, to wild native shrimp populations. The
principles of HACCP, in conjunction with International Council for
Explorations of the Sea and the European Inland Fisheries Advisory
Commission Codes of Practice, were proposed to control the spread of exotic
animal viruses into the environment. Shrimp aquaculture has the following
proposed critical control points: pond site selection; water supply
quality; pond management techniques; and transportation, especially as it
relates to the live transport of aquaculture shrimp species (21).
Approximately 600 million pounds of shrimp are also imported for further
processing into the United States on a yearly basis, half of which are
aquacultured species (3). Natural resource managers, particularly at the
state level, are concerned about the possible transmission of exotic shrimp
pathogens into the environment from shrimp processing plant wastewater
discharge and solid waste material landfill leakage. Proposed HACCP shrimp
processing plant critical control points include unload/receive;
de-ice/wash; thaw; dehead/peel/devein; wash; re-ice; de-ice/wash; re-ice;
and dip/glaze (21).
Application of HACCP principles at aquaculture site and processing plant
locations has the potential to control transmission of exotic human and
animal pathogens. However, to our knowledge, except for the application of
HACCP principl
es to control of human pathogens in Asia (17), no research
has been conducted on this issue.
Address for correspondence: Michael Jahncke, Virginia Tech Seafood Research
and Extension Center, 102 King Street, P.O. Box 369, Hampton, VA 23669 USA;
fax: 757-727-4871; e-mail: mjahncke@vt.edu.
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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA