Antibiotic use in shrimp farming and implications for environmental impacts and human health

Abstract

Summary The use of antibiotics in aquaculture may cause development of antibiotic resistance among pathogens infecting cultured animals and humans. However, this is a recent issue and has not yet been thoroughly investigated. Furthermore, there is limited knowledge about the environmental effects of antibiotic use in aquaculture. It is well known that antibiotics are commonly used in shrimp farming to prevent or treat disease outbreaks, but there is little published documentation on details of usage patterns. This study, conducted in 2000, shows that a large proportion of shrimp farmers along the Thai coast used antibiotics in their farms. Of the seventy-six farmers interviewed, 74% used antibiotics in shrimp pond management. Most farmers used them prophylactically, some on a daily basis, and at least thirteen different antibiotics were used. Many farmers were not well informed about efficient and safe application practices. A more restrictive use of antibiotics could have positive effects for the individual farmer and, simultaneously, decrease impacts on regional human medicine and adjacent coastal ecosystems. It is likely that dissemination of information could contribute to a decreased use of antibiotics, without decreasing the level of shrimp production.

Full text

Antibiotic use in shrimp farming and implications for
environmental impacts and human health
Katrin Holmstr€
oom,
1,2
Sara Gra
¨slund,
1,2,
* Ann Wahlstr€
oom,
1,2
Somlak Poungshompoo,
3
Bengt-Erik Bengtsson,
2
& Nils Kautsky
1
1 Department of Systems Ecology, Stockholm University, SE-106 91 Stockholm, Sweden
2 Institute of Applied Environmental Research, Stockholm University, SE-106 91 Stockholm, Sweden
3 Faculty of Veterinary Science, Chulalongkorn University, Henri-Dunant Road, 10330 Bangkok, Thailand
(Received 31 December 2001; Accepted in revised form 24 June 2002)
Summary The use of antibiotics in aquaculture may cause development of antibiotic resistance
among pathogens infecting cultured animals and humans. However, this is a recent issue
and has not yet been thoroughly investigated. Furthermore, there is limited knowledge
about the environmental effects of antibiotic use in aquaculture. It is well known that
antibiotics are commonly used in shrimp farming to prevent or treat disease outbreaks, but
there is little published documentation on details of usage patterns. This study, conducted
in 2000, shows that a large proportion of shrimp farmers along the Thai coast used
antibiotics in their farms. Of the seventy-six farmers interviewed, 74% used antibiotics in
shrimp pond management. Most farmers used them prophylactically, some on a daily
basis, and at least thirteen different antibiotics were used. Many farmers were not well
informed about efficient and safe application practices. A more restrictive use of antibiotics
could have positive effects for the individual farmer and, simultaneously, decrease impacts
on regional human medicine and adjacent coastal ecosystems. It is likely that dissemination
of information could contribute to a decreased use of antibiotics, without decreasing the
level of shrimp production.
Keywords Antibiotic resistance, aquaculture, environment.
Introduction
It is widely recognized that the extensive use of
antibiotics in agricultural animal production con-
tributes to the development of antibiotic-resistant
pathogens and that these microbes can infect both
humans and domesticated animals (Khachatou-
rians, 1998; American Academy of Microbiology,
1999; Wegener et al., 1999; Willis, 2000). Given the
knowledge of resistance development it is possible
that similar problems may exist in connection
with the use of antibiotics in shrimp farming.
Development of resistant pathogens in aquaculture
environments is well-documented (Sørum, 1999;
Inglis, 2000), and evidence of transfer of resistance-
encoding plasmids between aquaculture environ-
ments and humans has recently been presented
(Rhodes et al., 2000). Little is known about
toxicological effects of antibiotic use in aquacul-
ture on non-target organisms and the environment
(Weston, 1996), but recent studies have shown that
several antibiotics are moderately to highly acutely
toxic to aquatic organisms (Holten Lu
¨tzhøft et al.,
1999; Halling-Sørensen, 2000; Halling-Sørensen
et al., 2000; Wollenberger et al., 2000). Shrimp
farming has boomed in tropical and subtropical
regions since the early 1980s and Southeast Asia is
the leading region. Thailand is the world’s largest
producer of cultured shrimps, yielding 235 000–
275 000 tons annually since 1993 (FAO, 2001).
Indonesia, the Philippines and Vietnam are also
among the top ten producers in the world (FAO,
2001). Most of the production in these countries is
exported, generating large amounts of foreign
exchange. In Thailand there are about 20 000
*Correspondent: Fax: +46 8158417;
e-mail: sara@ecology.su.se
International Journal of Food Science and Technology 2003, 38, 255–266 255
2003 Blackwell Publishing Ltd

shrimp farms covering about 80 000 ha, mainly
along the coasts (Rosenberry, 1999; Bangkok Post,
2001; The Nation, 2001). To illustrate these figures,
Barraclough & Finger-Stich (1996) calculated that
if the 80 000 ha of farms were spread out evenly
along the entire 2600 km of the coast of Thailand,
they would form a continuous belt that would be
about 300 m wide. The management practices in
these vast areas of farmland are likely to impact the
coastal environment in one way or another.
There is limited documentation in the interna-
tional literature on the use of antibiotics in Thai
shrimp farming, or in Southeast Asia as a whole
(Primavera et al., 1993; GESAMP, 1997; Cruz-
Lacierda et al., 2000; Phillips, 2000; Shariff et al.,
2000; Supriyadi & Rukyani, 2000; Tonguthai,
2000; Gra
¨slund & Bengtsson, 2001). The aim of
this study was to provide information on the use
of antibiotics in intensive Thai marine and
brackish water (hereafter collectively called mar-
ine) shrimp farming, and to briefly discuss the
hazards and risks for the environment and human
health caused by these management practices.
Thailand was chosen for this study because it is
the major producer of farmed shrimps, and also
because much research on how to achieve a
sustainable shrimp production is done within the
country. Many other countries that produce
farmed shrimps may possibly be in a similar
situation.
Methods
Interviews were conducted during April–May
2000 with the help of a Thai interpreter translating
between Thai and English. Altogether seventy-six
farm owners (56%) or farm managers (44%)
(hereafter collectively called farmers) were inter-
viewed in three different regions (Fig. 1). The
farmers participating in the study gave informed
consent. The farms included in the study were
intensive or semi-intensive farms culturing the
marine black tiger shrimp Penaeus monodon. The
farms were selected as randomly as possible within
each area. The interviews were based on an
extensive questionnaire regarding management
practices and the use of chemicals on the farm.
Interviews were conducted openly, with follow-up
discussions if necessary. Three regions with
important shrimp farming activities were included
in the study: the eastern Gulf Coast, the Andaman
Coast and the southern Gulf Coast. Along the
eastern Gulf Coast thirty farmers were inter-
viewed. A few of these were located inland, but
most of them were coastal. Twenty-four farmers
along the Andaman Coast and twenty-two farm-
ers along the southern Gulf Coast were inter-
viewed in the study. The farms visited were spread
out within each area. In this text, the word
antibiotic refers to both biologically and synthet-
ically produced compounds.
Results
Type of farms included in the study
At least sixty-nine of the seventy-six farms inclu-
ded in the study were intensively managed. They
either fulfilled the criteria used by Primavera
(1998) – stocking density 10–50 postlarvae per
square metre; pond area 0.1–1 ha; and a produc-
tion of 3–6 tons ha
)1
crop – or they had an even
higher stocking density or production rate. Two
farms in the eastern Gulf Coast area had a lower
production rate, and for the remaining five farms
there was insufficient information on stocking
density, pond area and/or production rate to
permit this kind of classification.
Thailand
Bangkok
Gulf of Thailand
Malaysia
Cambodia
Vietnam
N
108 ˚E
0 100 200 Kilometres
100 ˚E
6 ˚N
Myanmar
12 ˚N
a
b
c
Figure 1 Map of Thailand indicating the three areas where
the interviews were conducted. a, Eastern Gulf Coast,
b, Andaman Coast, c, Southern Gulf Coast.
Antibiotic use in shrimp farming K. Holmstr €
oom et al.256
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Use of antibiotics
About 74% of the farmers in the study used
antibiotics in pond management. The practice was
most widespread along the Andaman Coast where
92% of the farmers used antibiotics. Comparable
figures for the southern Gulf Coast were 82%, and
for the eastern Gulf Coast, 53% (Table 1). A
minimum of thirteen different known antibiotics
were used by the farmers and additionally about
ten were documented but not identified (Table 2).
The most commonly used antibiotics were norfl-
oxacin, oxytetracycline, enrofloxacin and different
sulphonamides. Of the farm owners interviewed,
67% used antibiotics, whereas the corresponding
figure for the managers was 85%. This tendency
was seen in both the eastern Gulf Coast area and
the southern Gulf Coast area, whereas at the
Andaman Coast a larger proportion of farm
owners than managers used antibiotics.
Prophylactic use of antibiotics turned out to be
very common. Of the farmers who used antibiot-
ics, 86% used them in preventive management, as
well as to treat disease when symptoms had arisen.
Farmers either used higher doses or what they
considered to be more potent antibiotics for
treatment rather than for prevention. Of the
farmers who used antibiotics in farm management,
14% distributed them daily to the shrimps. Many
of the farmers participating in the study did not
have sufficient information on efficient use of
antibiotics. For example, 27% of all farmers who
used antibiotics used them to prevent or treat viral
diseases such as white spot disease.
It was difficult to document the quantity of
antibiotics used in terms of volume or weight.
Only a few farmers gave detailed information on
the doses of antibiotics they used. These farmers
used enrofloxacin and/or norfloxacin for disease
treatment in the range of 0.5–6 g kg
)1
feed three
times a day for 1 week. For disease treatment, a
majority of the farmers applied the antibiotic
several times a day for 3–7 days, most commonly
7 days. The antibiotics were generally in a powder
form that was mixed with the feed and thrown
manually into the water. A few farmers mentioned
withdrawal periods for antibiotics, but this infor-
mation was not specifically requested during the
interviews, and more farmers may have been
aware of the importance of such measures.
It is possible that some of the commercial feed
used in the farms contained antibiotics. Flaherty
et al. (2000) reported that most commercial
shrimp feeds are enriched with antibiotics. How-
ever, this was not mentioned by any of the
seventy-six farmers we surveyed. A majority of
the shrimp farmers in the survey (at least 78%)
used shrimp feed from Charoen Pokphand (CP).
According to the Investor Relations Office of
Charoen Pokphand Foods Plc., the company’s
shrimp feeds do not contain antibiotics. This
means that most of the farmers used feed not
enriched with antibiotics.
Farmers in the study frequently observed dis-
ease conditions affecting cultured shrimps; 86% of
farmers had experienced problems with bacterial
and/or viral disease outbreaks. Infections caused
by Vibrio bacteria and white spot virus were most
common. Ninety-one per cent of farmers stated
that shrimps were infected by other organisms, e.g.
the protozoa Zoothamnium or Ôcat hairÕalgae. In
the two areas in the south, 90–100% of the
farmers had experienced disease or pest problems,
whereas about 80% of the farmers in the eastern
Gulf Coast area had experienced disease or pest
problems.
Table 1 Antibiotic use by shrimp farmers in the study
Area
No. of farmers
interviewed (no.)
No. of farmers
using antibiotics (no., %)
Proportion of antibiotic users (%, proportion)
Preventive use Daily use As antiviral
Eastern Gulf Coast 30 16 (53) 81 (13/16) 25 (4/16) 25 (4/16)
Andaman Coast 24 22 (92) 91 (20/22) 14 (3/22) 23 (5/22)
Southern Gulf Coast 22 18 (82) 83 (15/18) 6 (1/18) 33 (6/18)
Total 76 56 (74) 86 (48/56) 14 (8/56) 27 (15/56)
Antibiotic use in shrimp farming K. Holmstr €
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Discussion
The study covers three widely different regions of
the country. After the initial boom in establishing
shrimp farms in the coastal provinces close to
Bangkok, farms were sequentially established
along the southern Gulf Coast, the eastern Gulf
Coast and the Andaman Coast (Huitric et al.,
2002). Considering the wide geographical range
covered, the shrimp farms included in this study
can be said to be fairly representative of intensive
marine P. monodon culture in Thailand. About
15–20% of the farms were located inland, all of
these in the eastern Gulf Coast area. Of the eighty
farmers we approached, only four did not agree to
be interviewed, and this was mostly due to time
constraints. In general, the farmers who partici-
pated in the study were open and willing to share
their experiences. The method of gathering infor-
mation through translated interviews may result in
errors regarding single details. However, this has
been taken into account throughout the study, and
we consider the overall conclusions presented here
to be accurate.
Patterns of use
Fewer farmers in the eastern Gulf Coast area used
antibiotics than farmers in the southern parts of
the country. This could be related to the slightly
smaller portion of farmers in the eastern Gulf
coast area that had experienced disease and pest
problems than in the two areas in the south.
Twelve of the farms in the eastern Gulf Coast area
were recently established (age 0–4 years), and of
these nine did not use antibiotics at all. In the
Group Compound
No. of users
(no. after
interpretation)
Possible
interpretations
Tetracyclines Chlortetracycline 1
Oxytetracycline 4 (16)
Tetracycline 2
Quinolones Quinolone (unspecified) 1
Ciprofloxacin 2
Enrofloxacin 9
Norfloxacin 29
Oxolinic acid 2
Perfloxacin 1
Sulphonamides Misc. sulpha drugs 9
Sulphamethazine 1
Other antibiotics Chloramphenicol 1 (2)
Gentamycin 3
Trimethoprim 1
Tiamulin 1
Unidentified
antibiotics
BH one 1
Cenoxacin 1 Cinoxacin?
Chlor-M 1 Chloramphenicol
Eno-s 1 Enofloxacin?
Farmocin 1
Fomiquine 2 Flumequine?
Gregacin 1 Coccidiostatica?
Opsy 3 Oxytetracycline
Oxy 9 Oxytetracycline
Rhodocide 1 Rhodomycin?
Seanox 100 1
Vibrocin 1 Vibramycin ?
WINOX-A 1
Unidentified product
name
5
Table 2 Types of antibiotics used
in the shrimp farms included in the
study
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other two areas, only five of the farms visited were
recently established, and one of these did not use
antibiotics. A recently established farm may have
a lower risk of disease outbreaks, as pond water
and sediment would still be fairly free from any
local accumulation of chemical and organic wastes
as well as pathogens from shrimp farming. The
smaller proportion of antibiotic users in this area
may also be due to low salinity in the ponds.
About half of the farms in this area were inland
farms with lower salinity, and thus with lower risk
of infection by bacteria thriving in marine water,
such as luminescent Vibrio bacteria. Another
difference between the farms visited in the eastern
Gulf Coast area and the other two areas was that
the density of farms in general seemed to be lower,
a factor that is likely to diminish the risk for
disease outbreaks (Kautsky et al., 2000).
Among the farmers who used antibiotics in
pond management, about 27% used them incor-
rectly to prevent or treat viral diseases (corres-
ponding to 20% of all farmers participating in the
study). It is possible that the risk of outbreaks of
virus infections could be decreased by avoiding
bacterial infections, as these could make shrimp
more vulnerable to viruses. However, this is not
certain, and if the preventive usage stimulates
resistance, the result may be contrary. Some
antibiotics are marketed for use against viral
diseases (e.g. Ôto reduce the severity of redbody
disease and yellowhead diseaseÕ), and many farm-
ers seemed to believe that antibiotics were directly
aimed at treating or preventing viral diseases. The
usage of probiotics was common among the
shrimp farmers in this study. Probiotics are
micro-organisms, often Bacillus spp., intentionally
added to the ponds, e.g. with the purpose to out-
compete the pathogenic bacteria and thereby
decrease the risk for disease outbreaks (Moriarty,
1998). However, 88% of the farmers using anti-
biotics also used probiotics. A few of these farmers
were aware that antibiotics are likely to reduce the
efficacy of these micro-organisms; however, most
of them were not. These examples imply that a
large proportion of farmers are insufficiently
informed about various diseases, and the mode
of action of antibiotics and probiotics. Further-
more, they may even be misled by producers and
salesmen of antibiotics or probiotics. Farmers in
the present study generally purchased antibiotics
from shops providing various chemicals for
shrimp farm management, sometimes after con-
sulting diagnostic services associated with the
seller.
Hazards and risks
The possible hazards from the use of antibiotics,
including the possible paths of development of
resistance are intertwined and complex. The
substances can potentially have adverse effects
on the shrimp farming system, e.g. through
development of resistance among shrimp patho-
gens, on adjacent ecosystems, e.g. through toxic
effects on aquatic organisms, and on human
health, e.g. through contact dermatitis or devel-
opment of resistant human pathogens. To make a
risk assessment, the level of occurrence of the
substance in question in the environment should
be calculated, and compared with concentrations
of the substance for which biological effects are
predicted to occur (Suter, 1993). It is beyond the
scope of this article to conduct risk assessments
for antibiotic substances in shrimp pond envi-
ronments. However, several of the antibiotics
used by the farmers in this study were commonly
applied, potentially persist in the environment
and are known to have adverse biological effects
(e.g. cause toxic effects or resistance develop-
ment) as discussed below, and thereby constitute
potential risks to the environment and human
health. These groups of antibiotics, e.g. fluoro-
quinolones, tetracyclines and sulphonamides,
ought to be studied further, with respect to the
environmental fate and biological effects in
shrimp pond environments and subsequently
subject to risk assessments.
Development of resistance
The pattern of antibiotic use among the farmers in
this survey indicates that there is a severe risk of
development of resistant bacterial strains. Factors
that are a particular risk for resistance develop-
ment are the prophylactic use of antibiotics
at subtherapeutic levels (American Academy of
Microbiology, 1999; Wegener et al., 1999; Inglis,
2000) and the use of antibiotics causing multiple
resistance (Threlfall et al., 2000). Resistance may
develop among human pathogens. This could
cause human health problems locally among the
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farmers, and contribute to the already severe
regional situation of development of antibiotic
resistance which is affecting human medicine. The
widespread use of fluoroquinolones among the
farmers in this study, e.g. norfloxacin and ciprofl-
oxacin, is a particular cause for concern, consid-
ering their importance for treatment of a broad
range of human pathogens (WHO, 1998). Another
risk is that resistance may develop among shrimp
pathogens and thereby increase the difficulty of
treating bacterial infections in shrimp ponds. The
development of resistant bacteria due to the use of
antibiotics in fish farming is well documented
(Bj€
oorklund et al., 1991; Herwig et al., 1997; Alder-
man & Hastings, 1998; Sørum, 1999; Schmidt
et al., 2000). Smith et al. (1994) argued that the use
of antibiotics in fish farming in industrialized
countries with temperate climate poses only a
small risk to human health, but also stated that
data was insufficient for definitive conclusions. The
aquaculture environment and human environment
can interact closely. Rhodes et al. (2000) have
demonstrated that dissemination of tetracycline
resistance-encoding plasmids between aquaculture
and humans has already occurred in Europe. The
risk from use of antibiotics in aquaculture in
developing countries in the tropics may be higher
than in industrialized countries in temperate
regions. Much shrimp culture has taken place in
areas where there is limited control of antibiotic
use (Alderman & Hastings, 1998), and where
human pathogens often occur in the marine
environment (Reilly & Twiddy, 1992). Further
factors, such as high organic loads, water tempera-
ture, pH and salinity, make the environment in
intensively managed tropical shrimp ponds favour-
able for growth of micro-organisms, such as
V. cholerae and Salmonella (Reilly & Twiddy, 1992).
Resistance to certain antibiotics (e.g. chloram-
phenicol, ciprofloxacin and tetracycline) is devel-
oping in human pathogens in Southeast Asia
(WHO, 2001). In Thailand, human pathogens
such as different pathogenic Salmonella species
(gasteroenteritis) and V. cholerae strains (gaster-
oenteritis and cholera) are commonly resistant to
various antibiotics, e.g. chloramphenicol, sul-
phamethoxazole+trimethoprim, and gentamycin
(Boonmar et al., 1998; Dalsgaard et al., 2000).
Important human pathogens, such as pathogenic
Salmonella and V. cholerae strains, have been
isolated from tropical Asian shrimp farms
(Reilly & Twiddy, 1992; Bhaskar et al., 1995;
Dalsgaard et al., 1995). Other human pathogens
that occur in marine waters or sediment are, for
example, Aeromonas hydrophila (soft tissue infec-
tions and bacteriaemia), and Plesiomonas shigello-
ides (gastroenteritis) (WHO, 1999). In a study of
fish ponds in Southeast Asia, Twiddy & Reilly
(1995) showed that antibiotic-resistant Salmonella,
A. hydrophila and P. shigelloides occurred in ponds
where antibiotics had been used routinely. Resis-
tance to tetracycline, oxytetracycline, furazolidone
and sulphamethoxazole+trimethoprim were most
common. Dalsgaard et al. (2000) demonstrated
that different pathogenic V. cholerae strains isola-
ted from Thai shrimp farms were resistant to
sulphonamides. Resistance-encoding plasmids and
transposons may disseminate from one bacterial
species to another, and thereby spread resistance
to pathogens not usually present in the aqua-
culture environment. For example, Rhodes et al.
(2000) showed that tetracycline resistance-enco-
ding plasmids have spread between different
Aeromonas species and Escherichia coli. Plasmid-
mediated resistance is common for most antibiot-
ics used by farmers in this study and recently it has
also been confirmed for quinolones (Martine
´z-
Martine
´zet al., 1998). Some antibiotics can cause
cross-resistance, i.e. when a single resistance
mechanism affects several antibiotics. For exam-
ple, both oxolinic acid and oxytetracycline can
separately cause multiple resistance to oxytetracy-
cline, oxolinic acid and furazolidone in marine
sediment (Nygaard et al., 1992).
One of the factors causing the major collapse of
Taiwanese shrimp farming in 1988 was the indis-
criminate use of antibiotics resulting in the devel-
opment of resistant strains of shrimp pathogens
(Lin, 1989). In a study by Tendencia & de la Pen
˜a
(2001), high rates of antibiotic resistance were
found among V. harveyi and other bacteria
isolated from shrimp ponds in the Philippines,
where antibiotics had been used. Resistance to
oxytetracycline, furazolidone, oxolinic acid and
chloramphenicol was most common, and multiple
resistance was widespread among many isolates.
In an Indian P. monodon hatchery, mass mortality
of postlarvae was caused by strains of V. harveyi
with multiple resistance to cotrimoxazole, chl-
oramphenicol, erythromycin and streptomycin
Antibiotic use in shrimp farming K. Holmstr €
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(Karunasagar et al., 1994). Of these compounds,
the first two had been regularly used in the
hatchery as prophylactics.
Of the farmers included in this study, only two
mentioned development of resistance against
antibiotics. However, the use of many different
antibiotics, frequent switching between different
types, combined with the common use of the
recently developed fluoroquinolones (e.g. norfl-
oxacin and enrofloxacin) may reflect a need to
change between different antibiotics as the path-
ogens develop resistance.
Occupational exposure
Farmers may be extensively exposed to antibiotics
when they mix them with feed and distribute the
feed in the ponds. Many of the farmers in this study
were aware of the risks with disinfectants and/or
pesticides, and about half of them used gloves or
facial masks while handling these chemicals. How-
ever, none of the farmers mentioned risks from
handling antibiotics, and many of them used their
bare hands to mix the antibiotics with the feed. It is
well known that contact dermatitis can occur with
exposure to some antibiotics, sulphonamides, for
example (Rice & Cohen, 1996). Moreover, the
antibiotic chloramphenicol can have severe health
effects, such as aplastic anaemia (Rang & Dale,
1987). There are documented cases of cattle and
sheep farmers who have died of aplastic anaemia as
a result of their use of chloramphenicol in animal
husbandry (Brown, 1989).
Potential effects on adjacent aquatic ecosystems
Bioaccumulation and toxic actions of antibiotics
used in shrimp farming should be considered as
many are both persistent and slightly to highly
acutely toxic (Table 3). Much of the antibiotics
distributed in the ponds may end up in the pond
water or sediment. Antibiotics can leach from the
feed pellets into the pond water before the pellets
are consumed by the shrimps (Inglis, 2000), while
some feed will be left uneaten on the pond bottom.
Antibiotics that are added to the pond environment
may remain in the sediment for months. Several of
the antibiotics can be persistent in aquatic envi-
ronments. For example, tetracyclines, oxolinic
acid, several sulpha drugs and trimethoprim are
all known to be persistent, with varying results in
degradation studies depending on temperature,
depth in sediment, etc. (Samuelsen, 1989; Gaval-
chin & Katz, 1994; Samuelsen et al., 1994; Hektoen
et al., 1995; Capone et al., 1996; Halling-Sørensen
et al., 1998, 2000; Weston, 2000). Other antibiotics
such as sulphadimethoxine and chloramphenicol
appear to be short-lived in marine sediments (Lai
et al., 1995; Capone et al., 1996). Norfloxacin and
enrofloxacin rapidly degrade photolytically in pure
water (Burhenne et al., 1997), but may behave
differently in aquaculture sediment.
Little information is available on the effects of
antibiotics on non-target organisms, especially in
marine environments. There is a possibility that
antibiotic residues in sediment can have an impact
on microbial activities, but this needs to be studied
further (Weston, 2000). Some recent studies show
that several of the antibiotics used in the present
study, e.g. ciprofloxacin, oxolinic acid, chlortetra-
cycline, oxytetracycline, tetracycline, tiamulin and
trimethoprim, are acutely toxic to algae and
aquatic invertebrates (Holten Lu
¨tzhøft et al.,
1999; Halling-Sørensen, 2000, Halling-Sørensen
et al., 2000; Wollenberger et al., 2000). Effects on
adjacent aquatic ecosystems may occur, especially
if there is a repeated flow of antibiotics from
several cycles of shrimp culture. It has been shown
that oxytetracycline and oxolinic acid can be
accumulated by wild fauna such as fish, mussels
and crabs (Bj€
oorklund et al., 1990; Samuelsen
et al., 1992; Capone et al., 1996). Although with-
drawal times can reduce consumer risks in farmed
shrimps, such measures do not protect local
communities from exposure to residues in wild
animals that are collected near farming areas.
Residues in cultured shrimps
National food authorities in many countries
regularly monitor levels of antibiotic residues in
food to compare them with the maximum residue
limits (MRL). Guidelines for governmental con-
trol programmes of veterinary drug residues in
food and recommended MRLs are continuously
developed by the Codex Alimentarius Commission
of the Food and Agriculture Organization of the
United Nations (FAO) and the World Health
Organization (WHO) (Codex Alimentarius Com-
mission, 2001). Authorities and organizations in
many countries have conducted analyses of anti-
biotic residues in tiger shrimps during the 1990s.
In a study conducted in 1990–91, over 1400
Antibiotic use in shrimp farming K. Holmstr €
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P. monodon were purchased in Bangkok markets
and analysed for certain tetracyclines, quinolones,
sulphonamides and penicillins (Saitanu et al.,
1994). Antibiotic residues were found in about
8% of the analysed shrimps. In the USA, analyses
for chloramphenicol in imported shrimps have
been conducted regularly. From 1992 to 1993, five
samples (3.2% of the samples tested) contained
measurable amounts of chloramphenicol. Three of
these samples were from Thailand and two were
from China (Weston, 1996). Thai authorities have
repeatedly analysed shrimps for export for their
possible content of antibiotics. In 1993, 24% of
the analysed shrimps were contaminated with
tetracycline, a number that fell to 5% after 4 years
(Bangkok Post, 2000). Still, there is widespread
concern that this improvement has not taken place
for the domestic market. Many shrimp processing
plants in Thailand conduct analyses of antibiotic
residues in shrimps, and, if they contain antibiotics,
they can either be rejected or sold on the domestic
market instead of being processed for export
(SSNC, 1999). However, the same study indicates
that this rarely happens as shrimp farmers gener-
ally comply with the proper withdrawal times for
antibiotics. In 1997, the Swedish National Food
Table 3 Usage and some ecotoxicological information about the antibiotics found in the study
Group Compound
Number of
users
Use in human
medicine
Rapidly degradable*
(rough estimates)
Examples of toxicity to
aquatic organisms†
Tetracyclines Chlortetracycline 1 Yes No
c
Acute II
l
Oxytetracycline 4 (16) Yes Yes-No
d,e
No
f
Acute II; Non-toxic
m,n
Tetracycline 2 Yes No
d
Acute II; Non-toxic
l,n
Quinolones Ciprofloxacin 2 Yes Yes–no
g
No
h
Acute II
g
Enrofloxacin 9 Mainly veterinary use.
Cross-resistance to
ciprofloxacin
a
Yes
i
Norfloxacin 29 Yes Yes
i
Oxolinic acid 2 Mainly veterinary use.
Cross-resistance to
oxytetracycline
b
No
d,f
Acute II
m,n
Perfloxacin 1 Yes
Sulpha drugs Misc. sulpha
drugs
9No
d,f
(sulphadiazine,
sulphamethoxazole,
sulphasalazine,
sulphatrimetoprim)
Yes
j
(sulfadimethoxine)
Acute II; Non-toxic
m,n
(sulphadiazine)
Sulphamethazine 1 Mainly veterinary use.
Other Chloramphenicol 1 (2) Yes Yes
k
Antibiotics
Gentamycin 3 Yes
Trimethoprim 1 Yes No
f,g
Acute II
m
Tiamulin 1 Mainly veterinary use. Acute I-III
l,n
a
Ministry of Agriculture, Fisheries & Food (1998);
b
Nygaard et al. (1992);
c
Gavalchin & Katz (1994);
d
Halling-Sørensen et al.
(1998);
e
Doi & Stoskopf (2000);
f
Hektoen et al. (1995);
g
Halling-Sørensen et al. (2000);
h
Kummerer et al. (2000);
i
Burhenne et al.
(1997);
j
Capone et al. (1996);
k
Lai et al. (1995);
l
Halling-Sørensen (2000);
m
Holten Lu
¨tzhøft et al. (1999);
n
Wollenberger et al.
(2000).
*Estimates are based on the referred degradation studies, and if the results indicate that the substance can be degraded in the
aquatic environment to a level >70% within 28 days.
†Criteria for the toxicity (OECD, 1998): LC
50
(96 h) for fish and/or EC
50
(48 h) for crustacea and/or EC
50
(72 or 96 h) for aquatic
plants.
Acute I: 61mgL
)1
; Acute II: >1–610 mg L
)1
; Acute III: >10–6100 mg L
)1
.
Antibiotic use in shrimp farming K. Holmstr €
oom et al.262
International Journal of Food Science and Technology 2003, 38, 255–266 2003 Blackwell Publishing Ltd

Administration performed analyses for tetracy-
clines, sulphonamides and quinolones on shrimps
from Thailand, China and Indonesia (Nordlander,
1998), but none of the consignments contai-
ned detectable levels of the antibiotics. In 2001,
authorities in a number of European countries
found residues of chloramphenicol in tiger shrimps
imported from China, Vietnam and Indonesia. As
a result, the European Commission decided that
every consignment of shrimps from these countries
must be analysed for antibiotic residues before
import to the European Union (European Com-
mission, 2001a,b).
Available regulations and recommendations
In 2000, the World Health Organization Report on
Infectious Diseases declared that antibiotic resist-
ance poses a severe threat to human health, and
that the problem is growing and global. A massive
effort is required and a reduction in the use of
antibiotics in animals is one of eight issues listed in
the call to action of WHO (WHO, 2000). Regard-
ing fisheries and aquaculture, FAO has developed
a Code of Conduct for Responsible Fisheries
(FAO, 1995). The Code and the connected guide-
lines state that preventive use of antibiotics in
aquaculture should be avoided as far as possible
and the use of antibiotics should be preferably
under veterinary supervision. Additionally, it has
declared that states should regulate the input of
chemicals in aquaculture that are hazardous to
human health and the environment, and that
marketing and use of drugs which have not been
certified for aquatic use should be strictly regula-
ted (FAO, 1995, 1997). A measure that is imple-
mented by some Thai shrimp farmers is the use of
withdrawal periods to clear the antibiotic residues
from shrimps, as recommended by Chan-
ratchakool et al. (1998). According to the Thai
Ministry of Public Health, the antibiotic chloram-
phenicol is not allowed in animal feed in Thailand
(Thai Ministry of Public Health, personal com-
munication). However, among the seventy-six
farmers interviewed in this study, chloramphenicol
was used by one or two farmers. This is not an
alarming number, but it nonetheless reflects the
difficulties in implementing existing regulations.
Clear information about existing governmental
regulations regarding use of antibiotics in aqua-
culture should be provided to antibiotic sellers and
shrimp farmers, and compliance ought to be
further controlled. To decrease the excessive use
of antibiotics the present regulations may be
strengthened by prohibiting prophylactic use of
antibiotics and allowing only a few antibiotics for
general use as treatment in shrimp farming, while
saving others for emergency use only. These
should be antibiotics that are not crucial in human
medicine, do not cause cross-resistance to such
drugs, and do not pose a risk by occupational
exposure. However, in order to implement these
regulations extensive efforts must be made to
disseminate more information. With or without a
strengthened regulation, dissemination of infor-
mation to the farmers about safe and relevant use
of antibiotics may be the most important and
effective measure to take. Chanratchakool et al.
(1998) have listed a number of recommendations
regarding antibiotic use in shrimp farming, e.g.
only use antibiotics to treat bacterial infections,
use antibiotics to which bacteria are sensitive, use
fresh antibiotics, careful handling of the products
considering human exposure, use of correct doses
and durations, and apply adequate withdrawal
periods. Further recommendations are, for exam-
ple, avoidance of oral therapy if the cultured
animals are inappetent, avoidance of repeated use
of the same antibiotic and blanket treatment for
prophylactic use, monitoring of resistance pat-
terns, avoidance of polypharmacy, and detailed
recording of use of antibiotics (Inglis, 2000).
By decreasing the use of antibiotics in shrimp
culture, it may be possible to decrease farmers’
expenses for drugs, the risk of development of
resistance among shrimp pathogens, the risk
of unhealthy occupational exposure, the risk of
resistance development among human pathogens
on a local and regional scale, and the risks of
negative effects on coastal ecosystems. The stake-
holders that benefit from the excessive use of
antibiotics are the manufacturers and retailers of
antibiotics. There are certainly manufacturers and
retailers who promote the use of antibiotics in
shrimp farming in a responsible way, but there
may also be those who take advantage of farmers’
limited knowledge of, for example, the mode of
actions of antibiotics and the risks of resistance
development, when marketing how their products
should be used safely and efficiently – information
Antibiotic use in shrimp farming K. Holmstr €
oom et al. 263
2003 Blackwell Publishing Ltd International Journal of Food Science and Technology 2003, 38, 255–266

that is presently not often provided on product
labels.
Conclusions
A large number of antibiotics are used in Thai
shrimp farming. They are used not only to treat
diseases but also for prophylaxis. The prophylactic
usage, the use of antibiotics used in human
medicine, and the persistent and toxic properties
of many of the antibiotics are all factors clearly
contributing to the risks of resistance development
and toxic actions influencing not only the envi-
ronment, but also human health on a regional
scale. It is likely that the use of antibiotics could be
significantly reduced without decreasing produc-
tion yields by disseminating information among
farmers about the safe and effective use of
antibiotics in shrimp farming.
Acknowledgments
We wish to thank Jim Enright for helping us with
practical arrangements, and Jurgenne Primavera
and Alan Reilly for valuable comments on an
earlier version of the manuscript. This study was
financially supported by Sida, the Swedish Inter-
national Development Cooperation Agency.
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