ARTICLE IN PRESS

Int. J. Hyg. Environ. Health 212 (2009) 369377

www.elsevier.de/ijheh

Aquaculture: Environmental, toxicological, and health issues

David W. Cole, Richard Cole, Steven J. Gaydos, Jon Gray, Greg Hyland,
Mark L. Jacques, Nicole Powell-Dunford, Charu Sawhney, William W. Au
Department of Preventive Medicine and Community Health, 700 Harborside Drive, University of Texas Medical Branch,
Galveston, TX 77555-1110, USA

Received 26 February 2008; received in revised form 10 July 2008; accepted 15 August 2008

Abstract
Aquaculture is one of the fastest growing food-producing sectors, supplying approximately 40% of the worlds sh
food. Besides such benet to the society, the industry does have its problems. There are occupational hazards and
safety concerns in the aquaculture industry. Some practices have caused environmental degradation. Public perception
to farmed sh is that they are cleaner than comparable wild sh. However, some farmed sh have much higher body
burden of natural and man-made toxic substances, e.g. antibiotics, pesticides, and persistent organic pollutants, than
wild sh. These contaminants in sh can pose health concerns to unsuspecting consumers, in particular pregnant or
nursing women. Regulations and international oversight for the aquaculture industry are extremely complex, with
several agencies regulating aquaculture practices, including site selection, pollution control, water quality, feed supply,
and food safety. Since the toxicological, environmental, and health concerns of aquaculture have not been adequately
reviewed recently, we are providing an updated review of the topic. Specically, concerns and recommendations for
improving the aquaculture industry, and for protection of the environment and the consumers will be concisely
presented.
r 2008 Elsevier GmbH. All rights reserved.

Keywords: Aquaculture; Fish; Nutrition; Occupational health; Pesticides; Public health

Introduction and salmon. Thus, one would recognize that aquacul-

Husbandry of aquatic organisms has been practiced
through the ages (Bardach et al., 1972). Oyster culture,
for instance, thrived in ancient Rome and Gaul
(Bardach et al., 1972). Humankind has always been in
search of more efcient food-production methods for
ever increasing human consumption. In addition, many
sh are produced in hatcheries for sport shing and
repletion of wild stock, such as trout, largemouth bass,
Corresponding author. Tel.: +1 409 772 1545;
fax: +1 409 772 9108.
E-mail address: William.au@utmb.edu (W.W. Au).
ture not only feeds the human population, but also
provides a vital service to replenish certain species.
Since the 1960s, aquaculture production have in-
creased dramatically due to much improved conditions
such as water quality, disease control, nutritionally
complete feeds, and the development of improved stocks
through selective breeding, hybridization, and the
application of molecular genetics technology (Stickney,
1994). Globally, farmed sh production more than
doubled from 1987 to 1997 at a rate of 9% per year
(Englehaupt, 2007) and aquaculture is becoming a
major industry that provides approximately 43% of
seafood to the consumers (FAO, 2006, 2007a). China

1438-4639/$ - see front matter r 2008 Elsevier GmbH. All rights reserved.
doi:10.1016/j.ijheh.2008.08.003
 ARTICLE IN PRESS
370 D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
remains the largest producer with reported sheries
production of 47.5 million tons in 2004 providing an
estimated domestic food supply of 28.4 kg per capita as
well as production for export and non-food purposes,
followed by India and the Philippines (FAO, 2006).
The United States (US) ranks third in the world in
consumption of seafood and eleventh in the world in
aquaculture production, therefore the US has histori-
cally had to rely on high levels of seafood imports
(Goldberg et al., 2001).
It may appear that aquaculture is highly benecial
and has no drawbacks but that is far from accurate. The
aquaculture industry, like other industries, has its share
of occupational hazards, safety concerns, and risks to
the individual health of the worker. There also exist
several deleterious effects on the environment from
aquaculture. Farmed sh, although presumably safer
from contamination than wild sh, have, in fact, higher
body burden of certain toxic chemicals that may present
health concerns to unsuspecting consumers. On the
other hand, a major benet of farmed sh is that they
provide a good and low-cost source of polyunsaturated
fatty acids (PUFAs) which can enhance cardiovascular
health in humans.
Regulations and international oversight for the
aquaculture industry are extremely complex, with
several agencies attempting to regulate aquaculture
practices, including site selection, pollution control,
water quality, feed supply, and food safety. These
practices differ from country to country and sometimes
between states and territories within a country. How-
ever, there are ongoing efforts to standardize practices
across borders and harmonize international regulations.
The concerns and recommendations for improving
the aquaculture industry are of constant interest. From
our literature search in PubMed, we recognized that
there are only a handful of review papers on the general
topic during the last two years. The majority of them,
however, focused on infection and microbiological
problems. Therefore, an updated review of environ-
mental, toxicological and health concerns of aquacul-
ture is needed. Our current review has also included
recent publications on the topic.
Genetic manipulation in aquaculture and the
ecological impact on the environment
The use of technologies and breeding programs has
generated aquaculture species that are both more
practical and economical to produce. For example,
male tilapia grows faster than females, making it the
preferred sex for commercial production. A YY male
genotype sires progeny that are nearly all males (Muir,
2005). In contrast, rainbow trout are selected for an all
female crop for better growth rate and less risk
of precocious maturity (Muir, 2005). Gynogenesis
inbreeds these female sh by using irradiated sperm so
the progeny have no paternal genes making an all female
generation (Halvorson and Quezada, 1999). Atlantic
salmon raised in British Colombia are sterile triploid
females to prevent their breeding with wild Pacic
salmon in the event of an escape (Hulata, 2001;
Reichhardt, 2000). Salmons are sterilized by heating or
providing a pressure shock to the eggs shortly after
fertilization to retain an extra set of chromosomes
(Reichhardt, 2000). Further sex-control technologies
include endocrine treatments for sex reversal (Hulata,
2001).
Potential environmental and genetic hazards exist if
modied sh are released into the wild, e.g. uninten-
tionally as a result of escape (Stokstad, 2002; Maury-
Brachet et al., 2008). These sh that are then introduced
into the wild may spread unique diseases and parasites
(Beveridge, 1990). An example is a recent report
indicating that sea lice from farmed salmon can possibly
cause certain native salmons in British Columbia to
plummet by 99% within eight years (Krkosek et al.,
2007).
The ecological impacts are also centered on heigh-
tened predation and altered population or ecosystem
secondary to the escaped shs activities (Goldberg
et al., 2001). The modied sh may become established
where that species was not previously present. For
instance, a sh genetically altered with antifreeze protein
could migrate upstream to a colder environment
where the wild species cannot survive and displace the
endogenous species. The genetically altered sh could
reproduce with the feral type resulting either in a more
robust sh that disrupts the environment or in poorly
t sh causing a gradual extinction of the species
(Goldberg et al., 2001).
The development of benecial transgenic organisms
requires the insertion of appropriate genes during the
blastocyst stage of embryonic development. Genes that
can provide highly desirable benets include: growth
hormone, freeze protection and disease resistant genes
(Halvorson and Quezada, 1999). Transgenic sh have
been produced in Atlantic salmon, Coho salmon,
Chinook salmon, rainbow trout, cutthroat trout, tilapia,
striped bass, channel catsh, common carp, and Indian
major carps (FAO, 2007b). For example, Aqua Bounty
Farms Inc., of Waltham Massachusetts has developed a
transgenic Atlantic salmon that can grow up to six times
as fast as ordinary farm-raised salmon after the
introducing of a growth hormone and promoter
sequences from a Chinook salmon (Stokstad, 2002).
Although commercial production of transgenic sh has
been seriously considered (Hu et al., 2007), transgenic
sh has not been approved by the US Food and Drug
Administration for human consumption yet (Muir and
 ARTICLE IN PRESS
D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
Howard, 1999; FAO, 2007b; Hallerman, Personal
communication).
Occupational hazards of aquaculture
The occupational hazards, safety concerns, and risks
to health in the aquaculture industry can vary con-
siderably based on the types of operation, scale of
production, and even the specic species of interest
(EFSA, 2005). In 2006, the non-fatal occupational
injury incidence rate for aquaculture (injuries per 100
full-time workers) was 6.8 (Survey of Occupational
Injuries and Illnesses, Bureau of Labor Statistics, USA).
In comparison, terrestrial crop production was 5.3 and
animal production was 7.8. Aquaculture occupational
hazards and risks to health can generally be categorized
into those concerning physical work hazards, chemical
and toxic exposures, and risks associated with infectious
disease.
Regarding the physical work environment, risks
concerning machinery and tool use are similar to that
of terrestrial agriculture. High-torque capacity tractors
used in aquaculture, for example, are subject to the same
roll-over protection (Occupational Safety and Health
Administration (OSHA) compliance standards) as farm
tractors (OSHA, 2007). Electrocution and high-voltage
electrical accidents are also of concern, particularly due
to the proximity of water (Durborow, 1999). Other
hazards might include drowning, musculoskeletal in-
juries from repetitive lifting of heavy cages and nets,
over-use injuries like tenosynovitis from repetitive
motion tasks, and long-term exposure in extreme
environments of sunlight, wind, cold, and water
(Douglas, 1995). Therefore, personal otation devices
(PFDs), thermal protection for cold environment and
foam-padded PFDs against chest and rib injuries are
needed (Douglas, 1995). Divers are also at risk for
decompression sickness. Such cases have been reported
with multiple descents and ascents (deemed yo-yo
diving) to clear dead sh from cages, even in relatively
shallow water of less than 20 m (Douglas, 1991).
Toxic exposures are of concern to aquaculture work-
ers because they can be exposed to unique and toxic
chemicals, e.g. Nesslers Reagent which is used to test
for the presence of ammonia contains potassium
hydroxide, mercuric iodide, and potassium iodide
(Durborow, 1999). Hydrogen sulde (H2S) occurs
naturally from organic breakdown, often during anae-
robic reactions on pond bottoms (Durborow, 1999).
H2S can cause anoxic brain injury and unconsciousness
at high levels and is predominantly a mucous membrane
and respiratory irritant at lower levels (Kuschner and
Blanc, 2007). In one unfortunate case, the autopsies of
three drowned aquaculture workers reveled sublethal
371
H2S levels, and this exposure was thought to have
contributed to their drownings (Durborow, 1999).
Toxicity information on products is typically focused
on single chemicals. In aquaculture, combining the use
of multiple toxic products can be a common practice.
Such practices can produce toxic by-products and
harmful gases from chemical reactions, and the health
risk to workers under this condition is not known.
There are health risks to workers associated with
microbial exposure and processes related to the preven-
tion of infectious diseases in aquaculture species. For
example, with respect to prevention, accidental auto-
inoculation or self-injection with antimicrobials, immu-
nizations, or veterinary biologics carries the potential to
produce a range of pathology in the worker from local
tissue reaction to full anaphylaxis (Douglas, 1995;
Durborow, 1999). Aquaculture workers can be exposed
to uncommon microbes including bacteria, viruses,
algae, and parasites potentially causing zoonotic disease
or emerging infections. For example, four separate
tilapia sh processors developed health complications
subsequent to infection with Streptococcus iniae, a sh
pathogen not previously reported to be a cause of
disease in humans (CDC, 1996; Garrett et al., 1997).
As published by Durborow (1999), many other sh
pathogens are known to be contagious to humans,
including several species of the genera Mycobacterium
and Vibrio (especially M. marinum, V. vulnificus, and
V. parahemolyticus), as well as species of Streptococcus,
Aeromonas, Erysipelothrix, and Pseudomonas. A more
inclusive list would also include parasites (nematodes,
trematodes, and ukes), protozoans, and dinoagellates.
Environmental impact from aquaculture
Environmental degradation from aquaculture prac-
tices has been reported. The negative effects include
organic pollution and eutrophication, a buildup of
excess nutrients (primarily organic nitrogen and phos-
phorus) and wastes in an ecosystem. These problems
together with chemical pollution can cause algal bloom,
depletion of oxygen, reduction in water quality, death of
corals and habitat destruction (Boesch et al., 2001;
Aubin, 2006). Certain microorganisms that thrive in this
adverse environment are directly harmful to sh through
biologic and neurologic toxins (Aubin, 2006). These
detrimental effects are usually localized to surrounding
regions and can be transitory. Therefore, good manage-
ment protocols can be used to minimize the effects, e.g.
situate net pens in areas with high natural ushing rates,
periodic fallowing between cycles of production, use of
seaweed biolters and use of mollusk-farming to remove
organic nitrogen from the water (Kaspar et al., 1985;
Chopin et al., 1999; Debruyn et al., 2006).
 ARTICLE IN PRESS
372 D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
A large quantity of wild-caught sh has been used as
feeds for aquaculture. However, when these forage sh
stocks are heavily harvested, it can directly affect marine
ecosystems negatively by the reduction of food available
for predators (Naylor et al., 2000). Therefore, alter-
native sources of feed are being considered.
Chemicals used in aquaculture can also cause pollu-
tion in the environment. These chemicals can come from
antibiotics, pesticides, herbicides, hormones, anesthetics,
pigments, minerals, and vitamins (Goldberg et al., 2001;
JSA, 2007). There is limited data on the extent of
antibiotic use by producers outside of the USA but they
may rely on antibiotics to a greater extent (Mellon et al.,
2001). A concern about antibiotic use is that it may
affect un-intended species leading to antibiotic resis-
tance and other toxic effects (Brown, 1989). This may
have been a reason why some pathogens have become
resistant to many drugs that are used in aquaculture
(Dixon, 2000). Herbicides are used to control aquatic
weeds, algal blooms, and fouling organisms. Net pen
operators often treat their nets with paints that contain
copper-based algaecide. These and other compounds
appear relatively safe when applied in approved condi-
tions; however, there are concerns that a spill of these
chemicals can cause irreversible damage to the environ-
ment (Eisler, 1998).
Diseases and parasites for aquaculture can be
deleterious in wild sh stock. Parasites may serve as a
host for other lethal diseases such as infectious salmon
anemia (ISA) which has been detected in both escaped
farmed and wild sh (FWS/NOAA, 2000). Another
example of parasite introductions into the environment
is sea lice which is a serious problem affecting salmon
farms and can also impact wild salmon migrating
through coastal waters (Finstad et al., 2000; Krkosek
et al., 2007).
A concern that attracts a lot of attention is the
alteration and destruction of natural habitats. Habitat
modication is an important aspect for increasing
aquaculture productivity. It includes direct habitat
conversion and predator-control programs (Goldberg
et al., 2001). In some areas, ow and composition
of rivers is altered because of the biological processes
of non-native species. Farmed species may feed on and
cause local extinction of certain plant and aquatic
species. Clustering or poor sitting of aquaculture
operations can also obstruct wild animals use of their
natural surroundings including the passage of migrating
sh (Goldberg et al., 2001). Other organisms may be
introduced or removed from areas of aquaculture
therefore transforming the environment food web and
overall cycle (Phillips, 1990).
Aquaculture has some environmentally positive ef-
fects as well. Aquaculture can reduce the dependence on
natural stocks as well as genetic conservation of
endangered species. Aquaculture is also useful in areas
of limited aquatic life, by enrichment of the local water
column. Aquaculture indirectly benets the environ-
mental by providing a method to convert agriculture
waste into high-quality sh protein, by enriching pond
mud for use as fertilizer and for improving soil quality
on crop land (Muir, 1999).
Nutritional value and comparison with wild
seafood
Fish muscle is an abundant source of PUFAs in the
human diet, especially n-3 and n-6, or more commonly
known as omega-3 and omega-6, fatty acids. It is
believed that two of the very long-chain omega-3 fatty
acids, eicosapentaenoic acid, and docosahexaenoic acid,
specically may lower the risk of coronary heart disease
in humans (van Vliet and Katan, 1990). Fish is the
major dietary source of these two important fatty acids
in humans. Therefore, the American Heart Association
(AHA) recommends that healthy adults eat at least two
servings of sh per week. The AHA also recommends
that individuals with coronary heart disease need 1 g of
combined eicosapentaenoic acid and docosahexaenoic
acid per day; while those who have elevated triglycerides
may need 24 g per day (AHA, 2007). Such benet from
sh consumption makes comparing the composition of
these fatty acids in sh muscle between wild and farmed
sh an important investigation.
Among trout, salmon and sea bass, higher levels of
benecial omega-3 to omega-6 fatty acid ratios were
found in farmed compared to wild sh (Suzuki et al.,
1986; van Vliet and Katan, 1990; Alasalvar et al., 2002).
In addition, the benecial fatty acid composition of
farmed sh can be increased through the manipulation
of their diet (Bell et al., 2001). For example, Alasalvar
et al. (2002) showed that feeding sh with feed
that contained higher levels monoenoic acids led to
higher levels of these fatty acids in sh tissues. Similar
observations were made with oleic acids (Alasalvar
et al., 2002). More recently, sh feeds have also included
the use of vegetable sources such as soybeans, rapeseed,
and wheat (Cahu et al., 2004). The benets and
limitations on nutritional values from the use of the
modied sh feed needs to be evaluated.
Another topic which has been scientically studied is
the area of trace mineral and vitamin contents in sh.
Nettleton and Exler (1992) reported that, among nsh,
the only difference across all species was greater niacin
content in raw samples of farmed versus wild trout. This
difference, however, was not seen among the corre-
sponding cooked samples of trout. Alasalvar et al.
(2002) examined several essential and non-essential
minerals in sh samples and found higher levels of Fe,
 ARTICLE IN PRESS
D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
Al, Ti, and V in wild sea bass compared to their farmed
counterparts.
Contamination in sh and health issues
Consumers may select farmed sh for meal as a
healthier and safer alternative to wild sh because
aquaculture is presumably located away from industries
that generate contaminated air and water. However,
consumers have been surprised to nd that several
natural and man-made toxic substances are at higher
concentrations in farmed than wild sh (Table 1). Some
examples of man-made contaminants in farmed sh are:
pesticides, polybrominated biphenol ethers (PBDE), and
polychlorinated biphenols (PCB) in salmon (Hites et al.,
2004a, b; Montory and Barra, 2006; Hayward et al.,
2007), PBDE and dioxin in catsh (Minh et al., 2006),
dioxin and PCB in turbot (Blanco et al., 2007), PCB in
sea bass (Carubelli et al., 2007) and PCB in all
investigated sh (Pinto et al., 2008).
Table 2 provides a summary of health risk associated
with toxic contaminates that have been found in sh.
For example, mercury contamination of sh was directly
responsible for Minamata disease (a cerebral palsy-like
disease) and has been linked with adverse neuro-
cognitive outcomes in populations with high sh
consumption (Davidson et al., 2006; Axelrad et al.,
2007; EPA, 2001, 2004). Although mercury contamina-
tion levels are no higher in farmed sh than in wild sh
(Easton et al., 2002; Hites et al., 2004a), their interactive
toxic effects with co-existing man-made contaminants
(as described earlier) are not known. Presumably, their
consumption during pregnancy can raise health risk in
the offspring, resulting in EPA guidance for sh
limitations during pregnancy (Behrman et al., 2004;
Table 1. Contaminants found in studies of aquaculture sh
vs. wild caught sh
Contaminant AC Wild AC4Wild AC only
Mercury XX
PAH X PCB-like contaminants in sh feed can be made by
Dioxin XX
O.P. XX
PCB XX
PBDE XX
Antibiotic X
X one study on contaminants of aquaculture vs. wild sh.
XX two studies.
AC aquacultured sh.
PAH polyaromatic hydrocarbons.
O.P. organophosphates.
PBDE polybrominated diphenyl ethers.
PCB polychlorinated biphenyl.
373
Table 2. Contaminates and known associated risks of
exposure
Contaminant Associated risks
Mercury Neuro-cognitive
PBDE Cognitive/endocrine
PCB Cancer/cognitive
Dioxin Cancer hormonal/immune
cardiovascular system
Antibiotics Cancer/antibiotic resistance
PBDE polybrominated diphenyl ethers.
PCB polychlorinated biphenyl.
Ford et al., 2001; EPA, 2004). PCBs have been linked to
memory impairments, as well as other endocrine and
cognitive abnormalities (Dewailly et al., 2007; Hites
et al., 2004a; Foran et al., 2005).
The nding of higher contaminant burden, especially
from multiple man-made chemicals, in farmed com-
pared to wild sh was surprising to consumers. From
various estimates, consumption of these farmed sh can
raise risk to health consequences such as cancer (Hites
et al., 2004a, b; Foran et al., 2005; Hastein et al., 2006;
Montory and Barra, 2006; Carubelli et al., 2007;
Dewailly et al., 2007). Such health risk may overshadow
the cardiovascular benets from the consumption of
certain farmed sh, especially for susceptible individuals
such as pregnant or nursing women. Consequently,
consumers should make informed decisions on the
number of sh meals per week and on a mixture of
wild and farmed sh.
Efforts have been made to identify the source of such
contaminations and to reduce the problem. It turns out
that the contaminations have often been traced to the
sh feeds because the contaminant levels in sh tissue
have been correlated (and biomagnied) with that in
the sh feed (Hites et al., 2004a, b; Blanco et al., 2007;
Pinto et al., 2008). Another source is the inappropriate
location of aquaculture at sites with high natural
contaminants, e.g. arsenic in farmed tilapia (Ling et al.,
2005; Jang et al., 2006). The obvious approach to
reduce the rst problem is to change and/or modify the
sh feed. For example, selected removal of dioxin and
employing partitioning and decontamination processes
(Oterhals and Nygard, 2008). Alternatively, contami-
nant burden can be reduced by feeding sh with
contaminant-free (and presumably more costly) feed
towards the end of the aquaculture time, by taking
advantage of the natural clearance of toxic chemicals
and growth dilution character of the farmed sh
(Brambilla et al., 2007). In addition, advisories can be
provided to consumers to limit the consumption of
certain sh, especially to susceptible people (EPA, 2004;
Kiljunen et al., 2007).
 ARTICLE IN PRESS
374 D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
A contaminant in farmed sh that also attracted
concern is antibiotic medication. Potentially maintain-
ing the health of farmed sh for the short term, these
antibiotics can be carcinogenic and may also lead to
antibiotic resistance in human consumers (FDA Import
Alert, 2007). The FDA recently banned the importation
of 5 species of farmed sh from China in June 2007
following determination that 15% were contaminated
with nitrofuran, malachite green, gentian violet, and/or
uoroquinolone antibiotics (FDA Press Conference,
2007; FDA Import Alert, 2007).
Regulations and international oversight of
industry
Regulations and international oversight for the
aquaculture industry are extremely complex, with
several agencies attempting to regulate site selection,
pollution control, water quality, feed supply, produc-
tion, and food safety (FAO, 2006, 2007a). These
practices differ from country to country and sometimes
between states and territories within a country. With the
industrys signicant growth in the last twenty years and
continued projected expansion, there are ongoing efforts
to standardize practices across borders.
In the US, there are as many as three departments,
eleven federal agencies directly and another 10 indirectly
involved in regulating aquaculture (DeVoe, 2007). The
three US government departments are Agriculture
(USDA), Commerce (DOC), and Interior (USDI). The
USDA monitors and eradicates infected animals, and
conducts research programs on vaccine development,
genetic improvement, reproduction, nutrition, environ-
mental compatibility, product safety, and quality
(FAO, 2007a, b). The major responsibilities for DOC
in aquaculture are: (1) minimization of environmental
impacts and development of standards; (2) development
of cost-effective, environmentally sound aquaculture
and hatchery technology; (3) growth and production of
marine species throughout their life cycle; (4) biotech-
nology to provide improved strains, sterile animals,
detection of pathogens, and development of vaccines
and other measures for controlling disease and parasites;
(5) technology transfer to industry and government
partners; and (6) coordination with management agen-
cies to identify areas appropriate for aquaculture
facilities and develop more efcient permitting proce-
dures (FAO, 2007a, b).
The USDI has two major programs: the Fish and
Wildlife Service that operates the National Fish
Hatchery System (NFHS) and the US Geological
Survey. Their major responsibilities include shery
conservation, habitat preservation, reduction of disease
and improvement of health of aquatic organisms (FAO,
2007a, b).
In order to ensure proper safety for imported
aquaculture products and internal sale, the Hazard
Analysis and Critical Control Points (HACCP) program
has been implemented in the US and European Union
(FAO, 2006). This program is also promoted by the
Food and Agriculture Organization of the United
Nations (FAO) and the World Health Organization
(WHO). FAO/WHO has published reports detailing
recommendations on how different international mar-
kets can abide by the HACCP program. The HACCP
program is a preventive approach to food safety. It
focuses on physical, chemical, and biological hazards
within the aquaculture process and implements actions,
known as critical control points, to reduce or eliminate
the hazard instead of only focusing on the nished
product. HACCP is based around seven established
principles: (1) conduct a hazard analysis; (2) identify
critical control points; (3) establish critical limits for
each critical control point; (4) establish critical point
monitoring requirements; (5) establish corrective ac-
tions; (6) establish record keeping procedures; and (7)
establish procedures for ensuring the HACCP program
is working as intended (Goldberg et al., 2001). The
HACCP system puts the responsibility of safe produc-
tion and distribution of food products on the aqua-
culture sector. Major markets, such as North America
and the European Union are requiring HACCP
implementation (FAO, 2006). There is a strong interna-
tional movement towards governments to adopt this
program for their seafood-production sectors. This
would provide the needed uniformity for aquaculture
markets around the world to ensure the safe importation
and exportation of its food products.
Conclusion and recommendations
The many benets of aquaculture provide a strong
and credible argument for its continued implementation.
For example, farmed sh provides high amount of
omega-3 fatty acid that can benet cardiovascular
health of consumers at a much lower cost than wild
sh (Mozzafarian and Rimm, 2006). On the other hand,
the industry does have it own shares of problems and
these are being addressed (FAO, 2007b). Aquaculture
operations have been shown to have caused signicant
environmental degradation and the threats continue to
be present. In addition, more attention needs to be paid
to its unique occupational hazards. Infection of workers
and natural species with organisms from farmed sh
should be proactively prevented. Comprehensive occu-
pational health and workplace safety programs need to
be better organized and extended around the world.
 ARTICLE IN PRESS
D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
Such programs should address the effective application
of primary prevention systems, personal protective
measures, health surveillance, standardized regulatory
guidelines, and sound management practices.
It was a surprise to consumers that farmed sh can
have higher concentrations of certain toxic chemicals,
especially man-made chemicals, than wild sh. The main
sources of contamination are from bioaccumulation via
sh feed and from location of aquaculture in contami-
nated areas. The former problems can potentially be
minimized by changing the sh feed and by advisories
on limiting the consumption of farmed sh, especially
for susceptible individuals such as pregnant or nursing
women.
The continued growth and diversication of the
aquaculture industry requires increasing numbers of
governmental policies and recommendations. The most
current policy, the HACCP which has been adapted by
the US and the European Union, puts the responsibility
of safe production and distribution of food products on
the aquaculture sector (FAO, 2006, 2007a, b). This
system would provide the needed uniformity for
aquaculture markets around the world to ensure the
safe importation and exportation of its food products.
Aquaculture continues to provide valuable food
supply and economic support for many countries. At
the same time, we must remind ourselves that even
though aquaculture provides many benets, we must
strive to preserve the environment we inhabit, and
continue to provide a safe and reliable source of food
that can also enhance the health of millions of people
globally.
Acknowledgement
This review is the product of a project resulting from
an Environmental Health and Toxicology Course in the
Master of Public Health program at the University of
Texas Medical Branch (UTMB) in Galveston, Texas,
USA. David W. Cole, M.D., Steven J. Gaydos, M.D.,
Jon Gray, M.D., Mark L. Jacques, M.D., Nicole
Powell-Dunford, M.D. are in the Army Aerospace
Medicine Residency program; Greg Hyland, M.D. is in
the Air Force Aerospace Medicine Residency program;
Richard W. Cole is in the UTMB Aerospace Medicine
Residency Program; and Charu Sawhney, D.O. is in the
UTMB General Preventive Medicine Residency Pro-
gram.
Disclaimer: The views, opinions, and/or citations in
this report are those of the authors and should not be
construed as ofcial Department of the Army, Depart-
ment of the Air Force, or the Department of Defense
position, policy or decision, unless so designated by
other ofcial documentations.
375
References
AHA (American Heart Association). Available online at
/http://www.americanheart.orgS (as of 15 September 2007).
Alasalvar, C., Taylor, K.D.A., Zubcov, E., Shahidi, F., Alexis,
M., 2002. Differentiation of cultured and wild sea bass
(Dicentrarchus labrax): total lipid content, fatty acid and
trace mineral composition. Food Chem. 79, 145150.
Aubin, J., 2006. Characterisation of the environmental impact
of a turbot (Scophthalmus maximus) re-circulating produc-
tion system using life cycle assessment. Aquaculture 261,
12591268.
Axelrad, Daniel A., Bellinger, David C., Ryan, Louise M.,
Woodruff, Tracey J., 2007. Doseresponse relationship of
prenatal mercury exposure and IQ: an integrative analysis
of epidemiologic data. Environ. Health Perspect. 115,
609615.
Bardach, J.E., Ryther, J.H., McLarney, W.O., 1972. The
farming and husbandry of fresh and marine organisms.
Aquaculture, 868875.
Behrman, Richard E., Kliegman, Robert M., Jenson, Hal B.,
2004. Nelson Textbook of Pediatrics, 17th ed. Saunders,
Philadelphia, Pennsylvania.
Bell, J.G., McEvoy, J., Tocher, D.R., McGhee, F., Campbell,
P.J., Sargent, J.R., 2001. Replacement of sh oil with
rapeseed oil in diets of Atlantic salmon (Salmo salar) affects
tissue lipid compositions and hepatocyte fatty acid meta-
bolism. J. Nutr. 131, 15351552.
Beveridge, M.C.M., 1990. A quantitative and qualitative
assessment of wastes from aquatic animal production.
Aquaculture and water quality. The World Aquaculture
Society.
Blanco, S.L., Sobrado, C., Quintela, C., Cabaleiro, S.,
Gonzalez, J.C., Vietites, J.M., 2007. Dietary uptake of
dioxin (PCDD/PCDFs) and dioxin-like PCBs in Spanish
aquacultured turbot (Psetta maxima). Food Addit. Con-
tam. 24, 421428.
Boesch, D.F., Burroughs, R.H., Baker, J.E., Mason, R.P.,
Rowe, C.L., Siefert, R.L., 2001. Marine Pollution in the
United States: Signicant Accomplishments, Future Chal-
lenges. Pew Oceans Commission, Arlington, Virginia.
Brambilla, G., Dellatte, E., Fochi, I., Iacovella, N., Miiero, R.,
diDomenico, A., 2007. Depletion of selected polychlori-
nated biphenyl, dibenzodioxin, and debenzofuran conge-
ners in farmed rainbow trout (Oncorhynchus mykiss): a
hint for safer sh farming. Chemosphere 66, 10191030.
Brown, J.H., 1989. Antibiotics: their use and abuse in
aquaculture. World Aquaculture 20, 3443.
Cahu, C., Salen, P., de Lorgeril, M., 2004. Farmed and wild
sh in the prevention of cardiovascular diseases: Assessing
the possible differences in lipid nutritional values. Nutr.
Metab. Cardiovasc. Dis. 14, 3441.
Carubelli, G., Fanelli, R., Mariani, G., Nichetti, S., Crosa, G.,
Calamari, D., Fattore, E., 2007. PCB contamination in
farmed and wild sea bass (Dicentrarchus labrax L.) from a
coastal wetland area in central Italy. Chemosphere 68,
16301635.
CDC (Centers for Disease Control and Prevention), 1996.
Invasive infection with Streptococcus iniae Ontario.
Morb. Mort. Wkly. Rep. 45, 650653.
 ARTICLE IN PRESS
376 D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
Chopin, T., Yarish, C., Wilkes, R., Belyea, E., Lu, S.,
Mathieson, A., 1999. Developing Porphyra/salmon inte-
grated aquaculture for bioremediation and diversication
of the aquaculture industry. J. Appl. Phycol. 11, 463472.
Davidson, P., Myers, G.J., Weiss, B., Shamlaye, C.F., Cox, C.,
2006. Commentary: prenatal methyl mercury exposure
from sh consumption and child development: a review
of evidence and perspectives from the Seychelles child
development study. Neuro. Tox. 27, 11061109.
Debruyn, A.M., Trudel, M., Eyding, N., Harding, J.,
McNally, H., Moutain, R., Orr, C., Urban, D., Verenitch,
S., Mazumder, A., 2006. Ecosystemic effects of salmon
farming increase mercury contamination in wild sh.
Environ. Sci. Technol. 40, 34893493.
DeVoe, R.M. Marine Aquaculture Regulation in the United
States: Environmental Policy and Management Issues.
UJNR Technical Report no. 24. South Carolina. Available
at: /http://nsgd.gso.uri.edu/tamu/tamuw95003/tamuw95003_
part1a.pdfS. (accessed November 30, 2007).
Dewailly, E., Ayotte, P., Lucas, M., Blanchet, C., 2007. Risk
and benets from consuming salmon and trout: a Canadian
perspective. Food Chem. Toxicol. 45, 13451349.
Dixon, B.A., 2000. Antibiotics. In: Stickney, R.R. (Ed.),
Encyclopedia of Aquaculture. Wiley, New York.
Douglas, J., 1991. Decompression sickness in sh farm
workers: a new occupational hazard. Br. Med. J. 302,
12441245.
Douglas, J., 1995. Salmon farming: occupational health in a
new rural industry. Occup. Med. 45, 8992.
Durborow, R., 1999. Health and safety concerns in sheries
and aquaculture. Occup. Med. 14, 373406.
Easton, M.D.L., Luszniak, D., Von der Geest, E., 2002.
Preliminary examination of contaminant loadings in
farmed salmon, wild salmon and commercial salmon feed.
Chemosphere 46, 10531074.
EFSA, 2005. The opinion of the scientic panel on con-
taminants in the food chain on a request from the European
Parliament related to the safety assessment of wild and
farmed sh. Question No. EFSA-Q-2004-22. Eur. Food
Saf. Auth. J. 236, 6680.
Eisler, R., 1998. Copper hazards to sh, wildlife, and
invertebrates: a synoptic review. US Geological Survey,
Biological Sciences Division, Biological Science Report,
USGS/BRD/BSR 19970002.
Englehaupt, E., 2007. Farming the deep blue sea. Environ. Sci.
Technol. 41, 41884191.
EPA, 2001. Water Quality Criterion for the Protection of
Human Health: Methylmercury EPA-823-R-01-001, 110.
EPA, 2004. What you need to know about mercury in sh and
shellsh: 2004 EPA and FDA advice for women who might
become pregnant, women who are pregnant, nursing
mothers, young children. Accessed 26 October 2007 at
/http://www.epa.gov/waterscience/shadvice/advice.htmlS.
FAO (Food and Agriculture Organization of the United
Nations). 2006. State of World Aquaculture 2006.
FAO Fisheries Technical Paper, No. 500. Rome, FAO
2006. Available at: /http://www.fao.org/docrep/009/a0874e/
a0874e00.htmS (accessed November 30, 2007).
FAO (Food and Agriculture Organization of the United
Nations). 2007a Fishery and Aquaculture Country Prole,
United States of America. Available at: /http://www.fao.
org//website/FIRetrieveAction.do?dom=countrysector&
xml=FI-CP_US.xml&lang=enS (accessed November 30,
2007).
FAO (Food and Agriculture Organization of the United
Nations). 2007b. Aquaculture new opportunities and a
cause for hope. Available at: /http://www.fao.org/focus/e/
sheries/aqua.htmS (accessed 30 November 2007).
FDA Import Alert 16131, 2007. Accessed 26 October 2007 at
/http://www.fda.gov/ora/ars/ora_import_ia16131.htmlS.
FDA Press Conference, 2007. Seafood Imported from China
FTS-HHS-FDA Moderator: Michael Herndon, June 28,
2007 1:00 pm CT. Accessed 26 October 2007 at /www.
fda.gov/bbs/transcripts/transcript062807.pdfS.
Finstad, B., Bjrn, P.A., Grimnes, A., Hvidsten, N.A.,
2000. Laboratory and eld investigations of salmon lice
(Lepeophtheirus salmonis [Kryer]) infestations on Atlantic
salmon (Salmo salar L.) post-smolts. Aquaculture Res. 31,
795803.
Foran, Jeffery A., Carpenter, David O., Hamilton, M. Coreen,
Knuth, Barbara A., Schwager, Steven J., 2005. Risk-based
consumption advice for farmed atlantic and wild pacic
salmon contaminated with dioxins and dioxin-like com-
pounds. Environ. Health Perspect. 113, 552555.
Ford, Marsha, Delaney, Kathleen A., Ling, Louis J., Erickson,
Timothy, 2001. Clinical Toxicology, rst ed. Saunders
Company, Philadelphia, Pennsylvania.
FWS/NOAA (Fish and Wildlife Service/National Oceanic and
Atmospheric Administration), 2000. Endangered and
threatened species; nal endangered status for a distinct
population segment of anadromous Atlantic salmon
(Salmon salar) in the Gulf of Maine. Fed. Regist. 65,
6945969483.
Garrett, E., Lima dos Santos, C., Jahncke, M., 1997. Public,
animal, and environmental health implications of aqua-
culture. Emerg. Infect. Dis. 3, 453457.
Goldberg, R.J., Elliott, M.S., Naylor, R.L., 2001. Marine
Aquaculture in the United States: Environmental Impacts
and Policy Options. Pew Oceans Commission, Arlington,
Virginia.
Hallerman, E.M., Personal communication. Blacksburg, VA,
USA.
Halvorson, H.O., Quezada, F., 1999. Increasing public
involvement in enriching our sh stocks through genetic
enhancement. Genet. Anal.: Biomol. Eng. 15, 7584.
Hastein, T., Hjeltnes, B., Lillehaug, A., Utne Skare, J.,
Berntssen, M., Lundebye, A.K., 2006. food safety hazards
that occur during the production stage: challenges for sh
farming and the shing industry. Rev. Sci. Technol. 25,
607625.
Hayward, D., Wong, J., Krynitsky, A.J., 2007. Polybromi-
nated diphenyl ethers and polychlorinated biphenyls in
commercially wild caught and farm-raised sh llets in the
United States. Environ. Res. 103, 4654.
Hites, R.A., Foran, J.A., Carpenter, D.O., Hamilton, M.C.,
Knuth, B.A., Schwager, S.J., 2004a. Global assessment of
organic contaminants in farmed salmon. Science 303,
226229.
Hites, R.A., Foran, J.A., Schwager, S.J., Knuth, B.A.,
Hamilton, M.C., Carpenter, D.O., 2004b. Global assessment
 ARTICLE IN PRESS
D.W. Cole et al. / Int. J. Hyg. Environ. Health 212 (2009) 369377
of polybrominated diphenyl ethers in farmed and wild
salmon. Environ. Sci. Technol. 38, 49454949.
Hu, W., Wang, Y., Zhu, Z., 2007. Progress in the evaluation of
transgenic sh for possible ecological risk and its contain-
ment strategies. Sci. China C. Life Sci. 50, 573579.
Hulata, G., 2001. Genetic manipulations in aquaculture: a
review of stock improvement by classical and modern
technologies. Genetica 111, 155173.
Jang, C.S., Liu, C.W., Lin, K.H., Huang, F.M., Wang, S.W.,
2006. Spatial analysis of potential carcinogenic risks
associated with ingesting arsenic in aquacultural tilapia
(Oreochromis mossambicus) in blackfoot disease hyperen-
demic areas. Environ. Sci. Technol. 40, 17071713.
JSA (Federal Joint Subcommittee on Aquaculture) 2007.
Working group on quality assurance in aquaculture produc-
tion: guide to drug, vaccine, and pesticide use in aquaculture,
April 2007 revision. /http://aquanic.org/jsa/wgqaap/
drugguide/Drug%20Guide%207-5-07.pdfS (accessed on 20
October 2007).
Kaspar, H.F., Gillespie, P.A., Boyer, I.C., MacKenzie, A.L.,
1985. Effects of mussel aquaculture on the nitrogen cycle
and benthic communities in kenepuru sound, marlborough
sounds, New Zealand. Mar. Biol. 85, 127136.
Kiljunen, M., Vanhatalo, M., Mantyniemi, S., Peltonen, H.,
Kuikka, S., Kiviranta, H., Parmanne, R., Tuomisto, J.T.,
Vuorinen, P.J., Hallikainen, A., Verta, M., Ponni, J.,
Jones, R.I., Karjalainen, J., 2007. Human dietary intake
of organochlorines from Baltic herring: implications of
individual sh variability and sheries management. Ambio
36, 257264.
Krkosek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A.,
Lewis, M.A., 2007. Declining wild salmon populations
in relation to parasites from farm salmon. Science 318,
17721775.
Kuschner, W., Blanc, P., 2007. Gases and other airborne
toxicants. In: LaDou, J. (Ed.), Occupational and Environ-
mental Medicine. McGraw Hill Medical, New York,
pp. 521522.
Ling, M.P., Liao, C.M., Tasi, J.w., Chen, B.C., 2005. A
PBTK/TD modeling-based approach can assess arsenic
bioaccumulation in farmed tilapia (Oreochromis mossam-
bicus) and human risks. Integr. Environ. Assess. Manage.
1, 4045.
Maury-Brachet, R., Rochard, E., Durrieu, G., Boudou, A.,
2008. The storm of the century (December 1999) and the
accidental escape of Siberian sturgeons (Acepenser baerii)
into the gironde estuary (Southwest France). An original
approach for metal contamination. Environ. Sci. Pollut.
Res. Int. 15, 8994.
Mellon, M., Benbrook, C., Benbrook, K.L., 2001. Hogging It!
Estimates of Antimicrobial Abuse in Livestock. Union of
Concerned Scientists, Cambridge, Massachusetts.
Minh, N.H., Minh, T.B., Kajiwara, N., Kunisue, T., Iwata,
H., Viet, P.H., Tu, N.P., Tuyen, B.C., Tanabe, S., 2006.
Contamination by poylbrominated diphenyl ethers and
persistent organochlorides in cathish and feed from
377
Mekong River Delta, Vietnam. Environ. Toxicol. Chem.
25, 27002708.
Montory, M., Barra, R., 2006. Preliminary data on poly-
brominated dephenyl ethers (PBDE) in farmed sh tissues
(Salmo salar) and sh feed in Southern Chile. Chemosphere
63, 12521260.
Mozzafarian, D., Rimm, E., 2006. Fish intake, contaminants,
and human health: evaluating the risks and the benets.
JAMA 296, 18851899.
Muir, J., 1999. The solution to pollution? The value and
limitations of environmental economics in guiding aqua-
culture development. Aquaculture Econ. Manage. 3, 4357.
Muir, J., 2005. Managing to harvest? Perspectives on the
potential of aquaculture. Philos. Trans. 360, 191218.
Muir, W.M., Howard, R.D., 1999. Possible ecological
risks of transgenic organism release when transgenes
affect mating success: Sexual selection and the Trojan
gene hypothesis. Proc. Natl. Acad. Sci. (USA) 96,
1385313856.
Naylor, R.L., Goldberg, R.J., Primavera, J.H., Kautsky, N.,
Beveridge, M.C.M., Clay, J., Folke, C., Lubchenco, J.,
Mooney, H., Troell, M., 2000. Effect of aquaculture on
world sh supplies. Nature 405, 10171024.
Nettleton, J.A., Exler, J., 1992. Nutrients in wild and farmed
sh and shellsh. J. Food Sci. 57, 257260.
OSHA (Occupational Safety and Health Administration),
2007. Standards 29 CFR, part 1928. /http://www.
osha.gov/pls/oshaweb/owadisp.show_document?p_table=
STANDARDS&p_id=10957S (accessed on 20 October
2007).
Oterhals, A., Nygard, E., 2008. Reduction of persistent
organic pollutants in shmeal: a feability study. J. Agric
Food Chem. 56, 20122020.
Phillips, M.J., 1990. Impact of aquaculture on water resources.
In: Brune, D.E., Tomasso, J.R. (Eds.), Aquaculture and
Water Quality. The World Aquaculture Society.
Pinto, B., Garritano, S.L., Cristofani, R., Ortaggi, G.,
Giuliano, A., amodio-Cocchierri, R., Cirillo, R., DeGiusti,
M., Boccia, A., Reali, D., 2008. Monitoring of polychlori-
nated biphenyl contamination and estrogenic activity in
water, commercial feed and farmed seafood. Environ.
Monit. Assess. 144, 445453.
Reichhardt, T., 2000. Will souped up salmon sink or swim?
Nature 406, 1012.
Stickney, R.R., 1994. Principles of Aquaculture. Wiley, New
York.
Stokstad, E., 2002. Engineered sh: friend or foe of the
environment? Science 297, 17971799.
Suzuki, H., Okazaki, K., Hayakawa, S., Wada, S., Tamura, S.,
1986. Inuence of commercial dietary fatty acids on
polyunsaturated fatty acids of cultured freshwater sh
and comparison with those of wild sh of the same species.
J. Agric. Food Chem. 34, 5860.
van Vliet, T., Katan, M.B., 1990. Lower ratio of n-3 to n-6
fatty acids in cultured than in wild sh. Am. J. Clin. Nutr.
51, 12.