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R E S E A R C H Open Access
Restrictions on antimicrobial use in food animal
production: an international regulatory
and economic survey
Dina Fine Maron
1,2
, Tyler JS Smith
1,2
and Keeve E Nachman
1,2,3*
Abstract
Background: The administration of antimicrobial drugs to food animals at low doses for extended durations for
growth promotion and disease prevention has been linked to the global health crisis of antimicrobial resistance.
Internationally, multiple jurisdictions have responded by restricting antimicrobial use for these purposes, and by
requiring a veterinary prescription to use these drugs in food animals. Opponents of these policies have argued
that restrictions have been detrimental to food animal production where they have been adopted.
Methods: We surveyed the antimicrobial use policies of 17 political jurisdictions outside of the United States with
respect to growth promotion, disease prevention, and veterinary oversight, and reviewed the available evidence
regarding their production impacts, including measures of animal health. Jurisdictions were included if they were a
top-five importer of a major U.S. food animal product in 2011, as differences between the policies of the U.S. and
other jurisdictions may lead to trade barriers to U.S. food animal product exports. Jurisdictions were also included if
information on their policies was publicly available in English. We searched the peer-reviewed and grey literatures
and corresponded with jurisdictions’U.S. embassies, regulators, and local experts.
Results: Jurisdictions were categorized by whether they prohibit use of antimicrobials for growth promotion and/
or use of antimicrobials without a veterinary prescription. Of the 17 jurisdictions surveyed, six jurisdictions have
prohibited both types of use, five jurisdictions have prohibited one use but not the other use, and five jurisdictions
have not prohibited either use, while information was not available for one jurisdiction. Data on the production
impacts of these prohibitions were limited, although available data, especially from Denmark and Sweden, suggest
that restrictions on growth promotion use can be implemented with minimal production consequences.
Conclusions: A majority of leading U.S. trade partners have more stringent policies regarding antibiotic use and
veterinary oversight in food animal production. Available data suggest that restrictions on growth promotion may
not be detrimental to production in the long run, although additional research could be useful. There is evidence
that discordance between the U.S. and other jurisdictions with respect to antimicrobial use in food animals may be
detrimental to U.S. access to export markets for food animal products. The available economic evidence
strengthens the rationale for restricting antimicrobial use in U.S. food animals.
Keywords: Antimicrobial, Antibiotic, Drug resistance, Bacteria, Food animal, Agriculture, Veterinarian, Trade
* Correspondence: knachman@jhsph.edu
1
Johns Hopkins Center for a Livable Future, Johns Hopkins University, 615 North
Wolfe Street, Suite W7010, Baltimore, MD 21205, USA
2
Department of Environmental Health Sciences, Bloomberg School of Public
Health, Johns Hopkins University, 615 North Wolfe Street, Baltimore, MD
21205, USA
Full list of author information is available at the end of the article
© 2013 Maron et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Maron et al. Globalization and Health 2013, 9:48
http://www.globalizationandhealth.com/content/9/1/48
Background
The dominant model of food animal production in the
United States and increasingly in other countries is char-
acterized by large-scale, high-throughput confinement
operations with herds or flocks that can range in size
from hundreds to hundreds of thousands of animals
[1,2]. These animals are typically supplied with drinking
water and grain-based feeds that may be amended with
antimicrobial and other drugs for multiple purposes [3].
In the U.S., antimicrobials are approved to treat, control,
and prevent disease in food animals, and for production
purposes like growth promotion [4]. Many antimicro-
bials are available without a veterinary prescription [4].
In the U.S., the quantity of antimicrobials sold for use in
food animals is approximately four times greater than
the quantity sold for use in humans [5,6].
The widespread use of antimicrobials in food animal
production has been linked to the development of anti-
microbial resistance (AMR) in bacterial populations; AMR
has emerged as a global health crisis [7]. When anti-
microbials are administered to food animals for disease
prevention or growth promotion, they are commonly ad-
ministered at lower doses and for longer durations than
when these drugs are used for disease treatment and con-
trol; administration of low doses for extended periods can
increase selective pressure for AMR [8,9]. In these cases,
antimicrobials are usually administered via medicated feed
or drinking water on a herd- or flock-wide basis, leading to
imprecise dosing when animals can choose what quantity
of feed or water to consume and potentially enhancing se-
lection for AMR [10]. Additionally, although veterinary
oversight of antimicrobial use has been associated with re-
duced selection for AMR [11,12], veterinary involvement
in the use of antimicrobials by the U.S. food animal indus-
try is often limited. For example, a U.S. Department of
Agriculture investigation found that only 46% of surveyed
dairy producers based antibiotic use for a common condi-
tion in dairy cows on veterinary recommendations [13].
There is evidence that modifying some current pro-
duction practices can limit food animal morbidity and
mortality despite reductions in antimicrobial use [14,15].
Multiple countries have restricted the use of antimicro-
bials for growth promotion and disease prevention and/
or required producers to obtain a veterinary prescription
to purchase or administer these drugs. In the U.S., pub-
lic health scientists and advocates have argued that, to
protect the efficacy of antimicrobials at treating human
diseases, all growth promotion uses and most prophylac-
tic uses should be phased out of U.S. food animal pro-
duction in favor of reforming production practices, and
that veterinary oversight of all antimicrobial use should
be required [16,17]. The U.S. Food and Drug Adminis-
tration (FDA) has initiated a process by which pharma-
ceutical companies may voluntarily withdraw approvals
to market antimicrobials for growth promotion and
amend approvals to market antimicrobials over the
counter so that a veterinary prescription or similar over-
sight is required for their purchase or use. The FDA has
resisted calls to use its regulatory authority to withdraw
these approvals, however, and has endorsed the contin-
ued use of antimicrobials for disease prevention [4]. This
approach has drawn criticism from public health advo-
cates, who promote countries with more restrictive pol-
icies as models for the U.S. to emulate [18,19].
The U.S. food animal and pharmaceutical industries
have opposed restrictions adopted outside of the U.S.
and have argued that such restrictions have been detri-
mental to food animal production where they have been
implemented [20,21]. The production impacts of these
policies have been discussed elsewhere to a limited ex-
tent [22], but we are unaware of any comprehensive re-
view of these restrictions or their impacts on production
in the peer-reviewed literature. This article surveys the
policies of political jurisdictions regarding the use of
antimicrobial drugs in food animal production. The
available data on how these policies have affected animal
health and the economic performance of these jurisdic-
tions’food animal industries are summarized by country.
Methods
Selection of political jurisdictions
In the U.S., antimicrobials are approved for use in the
production of commodities including: poultry, eggs,
pork, beef, and dairy products [23]. The fresh, chilled,
and frozen forms of these commodities were included in
this analysis, representing approximately 70% of U.S. ter-
restrial food animal product exports in 2011 [24]. Com-
modity data were obtained through the U.S. Department
of Agriculture’s Foreign Agricultural Service’s(FAS)
standard query search engine [24], which derives data
from the U.S. Census Bureau’s Foreign Trade Statistics.
This FAS data, characterized by the standard coding
used to classify international trade—the Harmonized
Commodity Description and Coding System (HS)—was
the best fit for this work due to its international
consistency, the accessibility of recent data, and the ease
of communicating with FAS experts in the U.S. As de-
fined here, “poultry”includes “poultry and products,”
encompassing broiler meat, turkey meat, other poultry
meat, live poultry, and miscellaneous poultry. “Pork”in-
cludes frozen, chilled, and fresh pork. “Beef”includes
beef and/or veal that may be fresh, chilled, or frozen.
“Eggs”includes eggs and egg products. “Dairy”includes
milk and dairy-related products, including: condensed
and evaporated milk, non-fat dry milk, dry whole milk
and cream, fluid milk and cream, yogurt and other
fermented milk, butter and milkfat, ice cream, cheese
and curd, casein, whey, and other dairy products.
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In recent years, multiple practices of the U.S. food ani-
mal industry, such as the use of exogenous hormones in
cattle and the use of antimicrobial rinses to clean poultry
carcasses, have led other countries to restrict the import
of U.S. food animal products [25,26]. The possibility of
similar barriers to U.S. products due to differences in
antimicrobial use policies between the U.S. and other ju-
risdictions has been raised [22]. We selected jurisdic-
tions based on their share of U.S. food animal product
exports in part to help evaluate the possibility of poten-
tial future restrictions on these exports due to anti-
microbial use.
We included jurisdictions listed by the U.S. Department
of Commerce as among the top five importers of U.S. food
animal products for at least one of the five included com-
modities in 2011 (Table 1). Jurisdictions were also included
if information on their antimicrobial use policies was pub-
licly available or we were able to obtain relevant informa-
tion through contact with food animal production experts
or government agencies of those countries. The EU was in-
cluded as an independent entity although some of its 27
member states may have tighter antimicrobial restrictions
or exemptions from EU policies. Several EU member states
with relevant policies are included separately.
Data collection on jurisdiction-specific policies
Available information on the included jurisdictions was
collected via full-text searches of PubMed using the search
terms “antimicrobial”and “livestock,”and/or “food pro-
duction”and/or “growth promotion,”alongside the names
of jurisdictions and commodities (poultry, chicken, turkey,
beef, pork, swine, pig, dairy, and eggs). We identified add-
itional articles by searching each article’s reference section.
We also searched the grey literature and examined juris-
dictions’regulatory websites for relevant information.
Additional information was obtained through direct con-
tact with food animal production policy experts identified
through their authorship of papers on this topic or
through recommendations from other experts. We ini-
tially emailed or called embassies and/or jurisdiction-level
experts and asked them about their respective national
policies related to antimicrobial use for growth promotion
and veterinary prescription requirements. We later in-
quired about policies related to antimicrobial use for dis-
ease prevention and control, specifically.
We examined jurisdiction-specific policies that im-
pact the frequency of antimicrobial use for 1) produc-
tion purposes, such as growth promotion or improved
feed conversion, or 2) preventive reasons in the absence
of veterinarian-diagnosed disease. It is important to
recognize that the terminology used to characterize
antimicrobial use in policy settings is divisive, conten-
tious, and applied inconsistently. Given this, we endeav-
ored to gather data from jurisdictions that could best
describe their policies regarding these two contexts. In
doing so, we used the specific terminology in policy
documents or communications with jurisdiction-level
experts.
Two frequent inconsistencies in terminology require
clarification. The term antimicrobial refers to substances
that are capable of inhibiting or killing microorganisms.
Antibiotics are a subset of antimicrobials, and have trad-
itionally included only antimicrobials that were originally
derived from microorganisms. In our paper, we define
the term disease prevention as the prophylactic admi-
nistration of antimicrobials in the absence of disease.
We use the term disease control to refer to administra-
tion of antimicrobials to a group of animals to control
the spread of a disease when one or more individuals
within a flock or herd have been diagnosed with disease.
The presentation of information regarding jurisdiction-
specific policies varies in degree of detail because 1) un-
even levels of information were available regarding the
Table 1 The top 5 markets in 2011 for U.S. food
animal exports
Commodity Jurisdiction Sales
(in $1,000s)
% of U.S. export sales
for commodity
Dairy Mexico 1,165,916 24.4
Canada 444,149 9.3
China 361,993 7.6
Philippines 280,306 5.9
Japan 277,147 5.8
Poultry Mexico 912,570 16.2
Hong Kong 822,405 14.6
Canada 581,601 10.3
Russia 263,458 4.7
China 249,192 4.4
Pork Japan 1,884,048 40.2
Mexico 599,267 12.8
Canada 467,193 10.0
China 464,389 9.9
South Korea 433,277 9.2
Beef Canada 865,985 19.0
Mexico 760,606 16.7
Japan 758,696 16.6
South Korea 648,819 14.2
EU 227,394 5.0
Eggs Canada 74,691 17.2
Japan 72,462 16.6
EU 68,552 15.7
Mexico 42,310 9.7
Hong Kong 35,388 8.1
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intricacies of national policies and 2) there exists an in-
consistent degree of specificity in the actual policies. In
some instances we were not given access to a copy of the
regulations themselves, we were unable to access them in
English, or we were forced to rely upon potentially incom-
plete information. In this work we report on the available
national policies as they were reported to us. Provincial
policies were not included in our analysis.
The policies of the 17 political jurisdictions in this
work are classified by their antimicrobial restriction level
in this paper, organized into three tiers and then listed
in descending order by their contribution to overall
U.S. export market sales across the five commodities
(Table 2). Jurisdictions included in the Antimicrobial
Use Restricted category have banned the use of antimi-
crobials for growth promotion and require veterinary
prescriptions to use antimicrobials in food animals. The
Semi-Restricted category includes jurisdictions that have
a ban or partial ban on antimicrobial growth promoters
(AGPs) or require veterinary prescriptions. The No
Current Antimicrobial Use Restrictions category refers
to jurisdictions that have no AGP restrictions or veterin-
ary prescription requirements. For each jurisdiction, the
analysis provides an overview of its antimicrobial use
policies (including use-specific restrictions and veterin-
ary prescription policies), the implementation timeline
of these policies, and information on their production
impacts, as available.
No human or animal subjects were used in this re-
search. All persons consulted in the context of this study
were serving in an official capacity as appointed or
elected officials or as academic researchers; no personal
information was sought.
Results
Antimicrobial use restricted
European Union
EU-wide, limitations on antimicrobial use began in 1997
when the EU banned using avoparcin for growth promo-
tion [27]. In 1999, the bloc also banned growth promotion
uses of tylosin, spiramycin, bacitracin, virginiamycin,
carbadox, and olaquindox [27]. Remaining growth promo-
tion uses were banned in 2006 [27]. Although the EU re-
quires veterinary prescriptions to use antimicrobials in
food animals, it allows member states to grant exemptions
in certain cases. EU-wide information on the full eco-
nomic impact of this ban is not yet available
a
, although
some work has analyzed the specific economic impacts in
several member states that are discussed later in this
paper. The EU is an important export market for U.S. food
animal products. Annually, the U.S. exports approximately
$634 million of beef, pork, poultry, dairy, and eggs to the
EU, or 3.1% of U.S. export sales across these food com-
modities (Table 2).
Taiwan
In 2005, Taiwan amended its Veterinary Drugs Control
Act to ban AGPs and require veterinary prescriptions to
use antimicrobials in food animals, according to the
Taipei Economic and Cultural Representative Office in
the U.S. Antimicrobials may be used in food animals to
treat and prevent disease. Other information suggests
that Taiwan has been trying to phase out antimicrobials
for growth promotion but some antimicrobials are still
permitted for feed use. These documents were not avail-
able in English for us to verify. Taiwan accounts for ap-
proximately 2% of annual U.S. export sales of food
animal products, primarily in beef and poultry (Table 2).
Netherlands
In 1997, the Netherlands banned the antimicrobials
olaquindox and carbadox; concerns had been raised
about the carcinogenicity and genotoxicity of these
drugs [28,29]. Two years later, the country began moni-
toring AMR in food and animal pathogens through its
MARAN system [28]. Using MARAN data, it was
reported that total sales of antibiotics licensed for thera-
peutic use in the Netherlands declined by nearly 32%
(from 495 to 338 tonnes) between 2009 and 2011, sur-
passing a goal of a 20% reduction over that time period
[30]. Veterinary prescriptions are reportedly required to
use antimicrobials in food animals. We could not iden-
tify separate regulations pertaining to prophylactic anti-
microbial use. Approximately 1.2% of annual U.S. export
sales of food animal products are attributable to the
Netherlands (Table 2).
Germany
Germany banned avoparcin in 1996. Furthermore, in
addition to the 2006 EU-wide AGP ban, German law only
allows antibiotics to be used for the treatment of diseased
animals, not for growth promotion, and explicitly states
that antibiotics cannot be used for diseases that arise as a
result of “rearing conditions”[31]. Veterinary prescrip-
tions are required to administer antimicrobials.
In 2008, Germany enacted its own national antibiotic re-
sistance strategy, Deutsche Antibiotika-Resistenzstrategie
or “DART”. That strategy includes AMR monitoring, im-
proved data-sharing on resistance issues, and reducing
antibiotic use through better environmental prevention of
infectious diseases [32]. German state governments are re-
sponsible for assuring compliance [31].
In November 2011, Germany announced additional
measures to control antimicrobial use in food animal
production [31]. A central plank of this new effort is
better monitoring of the quantities of antibiotics pre-
scribed by veterinarians and the quantities actually con-
sumed by food animals. Germany will also collect data
on pharmaceutical use by the poultry industry for the
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Table 2 Antimicrobial use in food animals and U.S. export sales for 2011
Jurisdiction
ranked by U.S.
export market
sales ($)
National ban
on growth
promotion
National
veterinary
prescription
requirement
U.S. export sales for
5 commodities in
$1,000s (% U.S.
export market)
U.S. export sales for
poultry incl. eggs in
$1,000s
(metric tons)
U.S. export sales
for dairy in
$1,000s
(metric tons)
U.S. export sales
for pork in
$1,000s
(metric tons)
U.S. export sales
for beef in
$1,000s
(metric tons)
U.S. export sales
for eggs in $1,000s
(quantity in metric tons excl.
eggs measured in dozens)
a
Mexico Yes* Yes 3,438,395 (17.1) 912,570 (657,711) 1,165,916 (370,602) 599,267 (286,197) 760,606 (156,029) 42,310 (982)
Japan No Yes 3,071,017 (15.2) 151,126 (84,270) 277,147 (107,417) 1,884,048 (464,593) 758,696 (138,910) 72,462 (17,333)
Canada No No 2,358,928 (11.7) 581,601 (180,929) 444,149 (137,927) 467,193 (120,914) 865,985 (145,540) 74,691 (4,744)
South Korea N/D N/D 1,455,922 (7.2) 151,497 (112,965) 222,329 (68,634) 433,277 (148,577) 648,819 (135,553) 5,175 (1,794)
Hong Kong No Yes 1,148,403 (5.7) 822,405 (562,572) 21,461 (6,588) 86,527 (36,670) 218,010 (44,017) 35,388 (1,595)
China No No 1,075,574 (5.4) 249,192 (137,716) 361,993 (236,221) 464,389 (219,187) 0 (0) 4,362 (392)
Russia N/D N/D 676,944 (3.4) 263,458 (214,892) 2,720 (1,339) 198,074 (63,364) 212,692 (46,396) 14,600 (0)
EU Yes Yes* 623,908 (3.1) 238,386 (147,259) 135,298 (32,532) 23,183 (6,787) 227,041 (27,142) 68,552 (5,950)
Philippines N/D N/D 450,819 (2.2) 79,740 (75,791) 280,306 (83,739) 60,692 (29,369) 30,081 (6,790) 2,064 (659)
Taiwan Yes Yes 405,215 (2.0) 125,588 (104,941) 46,991 (18,363) 33,847 (14,583) 198,789 (35,354) 1,188 (282)
Australia No No 271,495 (1.4) 2,945 (644) 88,309 (32,564) 179,196 (56,059) 1,045 (178) 1,271 (183)
Netherlands** Yes Yes 235,935 (1.2) 38,465 (14,733) 54,138 (15,628) 8,692 (3,127) 134,640 (16,521) 11,390 (583)
Germany Yes Yes 57,751 (0.3) 24,939 (3,946) 6,662 (3,300) 4,642 (1,347) 21,508 (3,807) 21,098 (2,948)
Brazil No Yes 48,091 (0.2) 6,292 (69) 40,425 (22,356) 89 (11) 1,285 (273) 5,532 (18)
Ukraine No No 42,011 (0.2) 24,172 (11,745) 7,582 (2,344) 9,609 (3791) 648 (166) 11,604 (0)
Denmark Yes Yes 20,776 (0.1) 2,388 (487) 17,138 (3,736) 108 (24) 1,142 (187) 2,287 (445)
Sweden Yes Yes 7,768 (<0.1) 4,875 (1,138) 2,855 (716) 0 (0) 38 (6) 4,838 (1,137)
Data for this table were collected from Global Agriculture Trade Statistics in June 2012. Since data collection, some data may have been revised by USDA/FAS.
N/D=No Data.
* = with exceptions.
**= calculations include Netherlands Antilles.
a
For egg exports, USDA/FAS measures quantities in two ways: 1) by metric ton (for eggs not sold in dozens) and 2) in dozens (for eggs sold in dozens). For consistency with other categories, we include only the
quantity of egg exports reported by metric ton.
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first time. As a result of these provisions, the government
expects to be able to track pharmaceutical use to individ-
ual animals [31]. Germany is expected to release data on
overall quantities of pharmaceuticals used, including a
geographic breakdown of veterinary antibiotic use. These
new data will facilitate analyses of potential links between
antibiotic use and resistance [31].
In February 2013, the German Bundestag (the lower
house of the German parliament) passed a bill to require
livestock producers to report regularly antibiotic use to
German state governments [33]. The federal government
would then use these reports to develop averages for
antibiotic use. Producers that use antibiotics in excess of
these averages would have their use policies reviewed by
a veterinary authority, which would be empowered to
direct the producer to adopt alternatives to antibiotic
use. The measure must be passed by the Bundesrat (the
upper house) before its enactment into law. Germany
accounts for 0.3% of annual U.S. export sales of food
animal products (Table 2).
Denmark
Denmark was an early adopter of antimicrobial control
policies [27]. In 2000, it instituted a comprehensive na-
tional ban on AGP use, pre-dating the final EU-wide ban
by six years [27]. The country also requires veterinary
prescriptions to use antibiotics in food animals [27].
The first step toward Denmark’s ban on AGPs came in
1995 when Denmark banned avoparcin. In the same
year, the Danish government placed a monetary cap on
veterinarians’profits from antibiotic sales. This removed
an incentive for veterinarians to prescribe antimicrobials
[27]. In 1998, the Danish poultry industry voluntarily
stopped using AGPs [34]. Denmark’s swine producers
also halted AGP use in finishing pigs before the national
ban took effect [27,34]. From 1996–2003, the total use
of antimicrobials in animals declined by 35%, although
annual therapeutic use roughly doubled, due in large
part to increased use in weaning pigs [35]. In 2010, the
Danish swine industry adopted a voluntary ban on the
use of third-generation cephalosporins [36].
Beyond these bans, Denmark has taken additional mea-
sures to limit antimicrobial use. In 2002, Denmark pro-
hibited veterinarians from using fluoroquinolones except
in cases where antimicrobial susceptibility testing of cli-
nical isolates indicated that no other antibiotic could ren-
der effective treatment [27]. When fluoroquinolones are
utilized, government officials must be notified. Three years
later, in 2005, Denmark initiated biannual audits of the
practices of swine veterinarians, eventually including all
food-animal veterinarians [27]. In 2010, after observing an
uptick in antibiotic use, the country initiated its “yellow
card initiative,”which sets regulatory limits on antibiotic
use based on the size of a swine farm, shifting the burden
for minimizing antibiotic use from veterinarians to
farmers [27,34]. Danish government officials report that
since the initiative was implemented antibiotic use in food
animal production has dropped by 25% [27].
In general, efforts to eliminate AGP use in poultry were
implemented with few obstacles. The poultry industry had
altered its production practices in the 1990s to reduce the
occurrence of Salmonella infections in flocks; these
changes had already resulted in lower antimicrobial use.
Swine producers, however, faced difficulties in weaning
piglets without antibiotics [27]. Danish producers reported
increased treatment of piglets for diarrhea in pigs immedi-
ately following the ban, although diarrhea was typically
not confirmed by veterinary or laboratory diagnosis [37].
Piglet mortality also increased but returned to previous
levels after 1 year [38]. From 1992–1998, production of
weaning pigs increased from 18.4 million pigs to 27.1
million pigs [34]. Ultimately, after the ban began, pro-
duction did not drop off, and the upward trend in
Danish swine production continued [14].
Compared to 1992, when antimicrobial use peaked,
2008 antimicrobial use in swine was down by half [14].
Poultry also did not experience long-term negative pro-
duction impacts from the ban on AGPs, apart from a
small increase in the feed-conversion ratio [39]. Danish in-
dustry representatives now report that changes to their
production practices, such as later weaning, improved
diet, and lower stocking densities, minimized negative im-
pacts [27]. U.S. annual export sales to Denmark were $20
million in 2011, or about 0.1 percent of U.S. export sales
of food animal products (Table 2).
Sweden
Sweden was the first country to ban AGPs in food ani-
mal production. In 1986, it instituted a national ban on
AGPs and prohibited the use of antimicrobials absent a
veterinary prescription [40,41]. Sweden also stipulated
that antibiotics could only be used for “curing or
preventing disease”[40]. The impact of this AGP ban
was not uniform across animal species. The ban did not
lead to negative clinical or economic repercussions in
egg production since AGPs were not used in this area
before the ban [40]. By 1986, AGPs were also rarely used
in specialized beef production, so the ban did not result
in negative production impacts in that sector either [40].
In turkeys, where antimicrobials sometimes used for
growth promotion were reportedly only used to prevent
necrotic enteritis, the ban did not result in negative clinical
effects. Following the ban, broiler chicken producers were
still able to use antimicrobials to prevent and treat infec-
tions. The industry chose to administer virginiamycin
prophylactically to approximately 90% of broiler chickens
in the country. In 1988, virginiamycin was replaced with
penicillin, which was only administered in responses to
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outbreaks [40]. Reductions in broiler chicken production
were not observed, and the industry remains strong; total
production has nearly doubled in the 12 years following the
ban [40]. Although there were post-ban increases in thera-
peutic applications of antimicrobials to help prevent or
control outbreaks of necrotic enteritis for broiler chickens,
those numbers have since dropped [40].
Pig producers did report seeing some initial negative re-
sults from the ban. Prior to 1986, regimens of olaquindox
or mecadox were administered for growth promotion
until 10–12 weeks and then avoparcin or virginiamycin
regimens were administered to finishing pigs until slaugh-
ter at around 7 months [40]. While the health of finishing
pigs and the cost of producing them remained unchanged,
there were negative impacts among piglets. Piglet
mortality increased in the year following the ban by
1.5 %, it took 5–6 days longer for pigs to reach 25 kilo-
grams, and for the first four years following the ban,
antibiotic use at therapeutic doses increased [40,41].
While government data indicate that antibiotic use
dropped by approximately half by 1993, mortality and
production time for piglets remained slightly elevated
[41]. Compared to 1986–1987, 1997 average values for
post-weaning mortality were 1–2% less and the age at
25 kg was 3.5-4.5 days less [40]. We were unable to ob-
tain more recent information on these rates. In 2011,
Sweden was responsible for less than 0.1 percent of U.S.
export sales of food animal products (Table 2).
Antimicrobial use semi-restricted
Mexico
In 2007, Mexico enacted its Federal Law of Animal Health,
which restricts AGP use in animal feed and requires a vete-
rinary prescription to use antimicrobials in food animals.
The law banned most AGPs, but it provided exceptions
for 15 drugs, including: avoparcin, vancomycin, bacitracin,
tylosin, virginiamycin, avilamycin, bambermycin, spiramycin,
salinomycin, and monensin. There are no current plans to
phase out use of those drugs as growth promoters. Anti-
microbial disease prevention and control regulations were
unavailable in English. Mexico is the number one des-
tination point for U.S. food animal product exports, re-
sponsible for 17.1 percent of U.S. export sales of those
products annually (Table 2).
Japan
Japan does not have any restrictions on using antimicro-
bials for growth promotion, but its Food Safety Commis-
sion is reportedly considering restricting some uses of
antibiotics. A veterinary prescription is required for anti-
microbial use in food animals. Japan does not have any
regulations pertaining specifically to antimicrobial use
for the purposes of disease control and prevention. Japan
is the second largest market for U.S. exports of food
animal products, responsible for 15.2% of annual export
sales of those products (Table 2).
South Korea
We could not verify whether South Korea currently re-
stricts AGPs or requires a veterinary prescription to
use antimicrobials. In July 2010, however, South Korea
announced a ban on the “addition of antibiotics in ani-
mal feed…to strengthen the safety management of
domestic livestock products”[22]. This ban, geared to-
ward limiting the amount of drugs added into pre-
mixed animal feed, took effect in the second half of
2011. The ban is effectively a temporary hold on adding
any antibiotics into commercial compound feed until
a veterinary oversight system can be put into place,
representing the final step in a multi-year phase-out of
large-scale antibiotic additions without veterinary over-
sight [42]. Despite this targeted control effort, drugs
can still be added to food, water, and injected in food
animals on individual farms, but the addition of these
drugs must occur at the farm location [42]. Once a
veterinary oversight system is in place (reportedly ex-
pected no earlier than 2012, although we could not de-
termine whether this has since occurred) antibiotics
may be added into commercial compound feed at off-
farm feed mills [42]. South Korea is responsible for
7.2% of annual U.S. export sales of food animal pro-
ducts and is a major market for U.S. exports of beef
and pork (Table 2).
Hong Kong
Hong Kong does not have a comprehensive ban on
AGPs but a representative of its Agriculture, Fisheries
and Conservation Department states that Hong Kong
producers do not utilize AGPs due to breed selection
and the practice of bringing its animals to market at
a later date. Select AGPs, including avoparcin, were
banned in Hong Kong as of 2001. Veterinary prescrip-
tion for antibiotic use in animals is also required by law.
Hong Kong is responsible for 5.7% of annual U.S. export
sales of food animal products (Table 2).
Russia
We were not able to verify Russia’s official policies on
AGPs and veterinary prescription requirements. Media
reports document instances where Russia has turned
away meat imports because of its opposition to anti-
microbial rinses used by the U.S. food animal industry
[43]. Russia has regulations going into effect in July
2013 that may further limit antibiotic use though the
impacts of these regulations remain unclear [44]. Russia
is responsible for 3.4% of annual U.S. export sales of
food animal products (Table 2).
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No antimicrobial restrictions
A number of countries do not have any current restric-
tions on AGPs and only have limited requirements to ob-
tain veterinary prescriptions (Table 2). Canada, China
(excluding Hong Kong), Australia, Brazil and Ukraine
(listed in descending order of their financial contribution
to U.S. export sales of food animal products) do not have
any formal national restrictions on antimicrobial use for
the purposes of growth promotion. Canada and Australia
do report some limitations at the state or territory level.
Canada currently relies on voluntary actions to cur-
tail use for growth promotion. Requirements to obtain
veterinary prescriptions to use antimicrobials also vary
by province, and the country does not have separate
regulations for the use of antimicrobials for disease
prevention and control.
China does not have any restrictions on AGPs and
does not require veterinary prescriptions for antibiotic
use. Detailed information about AGP use in China is dif-
ficult to obtain, but in 2007, the scientist that oversees
China’s National Antibacterial Resistance Investigation
Net (NARIN), estimated that almost half of the 210,000
tons of antibiotics produced in China are administered
to animals via feed [45]. Brazil has not banned AGPs in
livestock production and there is no requirement to ob-
tain a veterinary prescription to use antibiotics in food
animals, according to a representative from its embassy.
Its regulations were not available in English. Ukraine has
not banned AGP use, but its embassy reports that anti-
biotics are not used to produce food animals in Ukraine.
Unknown
Philippines
We could not determine current policies in the Philippines
related to restrictions on antimicrobial use in food ani-
mals or veterinarian prescription requirements. Efforts
to communicate with Philippines officials were unsuc-
cessful. The Philippines are responsible for 2.2% of an-
nual U.S. food animal product export sales (Table 2).
Discussion
We examined the international regulatory landscape re-
lated to the use of antimicrobials in food animal produc-
tion. We sought to establish which jurisdictions have
national requirements that veterinarians oversee anti-
microbial use in food animals, and which jurisdictions
have restricted the use of antimicrobials in food animals
for growth promotion and, if information was available,
disease prevention and control. We were able to ascer-
tain answers to most of these questions for 17 political
jurisdictions, and found that there are varying levels of
antimicrobial controls in these settings, with restrictions
on AGPs being the most common.
Six jurisdictions have stringent restrictions on anti-
microbial use in food animal production. It is illegal to use
antimicrobials for growth promotion in those settings and
each requires a veterinary prescription to use antimicro-
bials in food animals. While the EU requires veterinary
prescriptions for antimicrobial use, it exempts some of its
27 member states. Separately, five jurisdictions have fewer
restrictions on antimicrobial use, with either full or partial
AGP bans or veterinary prescription requirements. Five
other jurisdictions do not have any restrictions on the use
of antimicrobials for growth promotion at the national
level or requirements to obtain veterinary prescriptions
for their use (Table 2).
While a ban on growth promotion has been central to
debates over antimicrobial use in the U.S., some jurisdic-
tions’policies have included more dynamic approaches as
well. Denmark’s yellow card initiative, for example, com-
bines robust surveillance of antimicrobial use with re-
quirements to implement alternative measures when
reported use is deemed excessive [27]. Proposed legisla-
tion in Germany would initiate a similar program [33].
These models recognize the importance of antimicrobials
to animal health and the need for clinical judgments by
qualified veterinarians, as well as the public health risks
posed by misuse of these drugs. Denmark has also taken
steps to limit financial conflicts of interest that may
incentivize veterinarians to prescribe antibiotics exces-
sively [27]. Neither approach has featured prominently in
U.S. policy debates. A barrier to their adoption in the U.S.
is the absence of a surveillance system for antimicrobial
use in food animals.
Data on impacts of antimicrobial use restrictions on
food animal production in these jurisdictions continue
to be limited. Most information comes from the expe-
riences of Denmark and Sweden, which were early
adopters of antimicrobial controls. Their respective pro-
ducers have suggested that stringent AGP controls can
be implemented with minimal economic consequences
for industry. Producers in Denmark and Sweden did not
report increased mortality or encounter other obstacles
in poultry, swine, beef and dairy products other than
those described in this work. Producers did report ele-
vated mortality and increased production time although
those increases have been reduced over time as manage-
ment practices have adapted [27,40,41].
Differences among jurisdictions with respect to food
animal production policies have threatened U.S. access
to export markets for these products. The EU has long
prohibited the importation of U.S. beef produced with
exogenous hormones, citing drug residues as a concern
[26]. The bloc currently permits the importation of a
limited quantity of beef derived from cattle certified by
the U.S. government as “non-hormone treated”[26].
While the economic impact of this restriction is difficult
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to estimate, initial losses were projected at approxi-
mately $100 million per year [26]. Since 1997, the EU
has also prohibited the importation of poultry processed
with antimicrobial rinses, arguing that such treatments
are less effective at reducing microbiological contamin-
ation than improved sanitation in production and pro-
cessing [25]. Before 1997, U.S. poultry exports to the 15
countries that then comprised the EU were valued at
$52 million; in 2011, poultry exports to those countries
were valued at $13 million [25].
Beyond the EU, Taiwan had banned beef and pork prod-
ucts with detectable residues of ractopamine, a growth
promotion and leanness drug used in the U.S. [46]. This
ban was subsequently revised to permit ractopamine re-
sidues in beef up to 10 ppb while maintaining a zero-
tolerance for ractopamine in pork [46]. U.S. access to the
Russian market has been hampered in recent years by
multiple issues, including antimicrobial drug residues
and antimicrobial rinses [47]. The U.S. has long main-
tained that restrictions adopted by the EU, Taiwan, and
Russia are not grounded in scientific evidence of human
health risk, and that they instead represent economic
protectionism [25,26,47].
Although international trade policies often hinge on
myriad factors—for example, the most recent restrictions
adopted by Russia appear to have been retaliation against
criticism of the country’s human rights record by the U.S.
Congress [48]—previous restrictions may still be instruct-
ive in the context of AMR. As concern over the contribu-
tion of food animal production to AMR in human
pathogens increases, efforts to limit U.S. food animal ex-
ports further may emerge. In 2011, the EU adopted a reso-
lution that called on its member states to “work towards
an international ban on antimicrobials as growth pro-
moters in animal feed, and to bring this matter up in its
bilateral negotiations with third countries such as the
United States”[22]. This suggests that, as with hormones
and antimicrobial rinses, the EU may view antimicrobial
use in food animals as a trade issue. Potential trade sanc-
tions against the U.S. would likely lead to long-term con-
sequences for the U.S. export market, stemming both
from declining production capacities during sanctions as
well as geographic dislocation of the market.
The World Trade Organization, which adjudicates trade
disputes between its member states, relies principally on
the opinions of the Codex Alimentarius Commission in
cases involving food safety [49]. In 2005, the Commission
published its “Code of Practice to Minimize and Contain
Antimicrobial Resistance”[50]. The Code states, “The re-
sponsible use of veterinary antimicrobial drugs in food-
producing animals…does not include the use for growth
promotion of veterinary antimicrobial drugs that belong
to or are able to cause cross resistance to classes of anti-
microbial agents used (or submitted for approval) in
humans in the absence of a risk analysis.”The Code also
calls for veterinary oversight of antimicrobial use and em-
phasizes alternatives to antimicrobial use for disease pre-
vention. In many cases, the current use of antimicrobials
in U.S. food animal production appears to be inconsistent
with these principles [16,51]. Although the FDA has
recommended that pharmaceutical companies voluntarily
withdraw approvals to market antimicrobials for growth
promotion and require veterinary oversight of their use
[4], the compliance of companies with these recommen-
dations is uncertain. The agency has not moved to restrict
antimicrobial use for disease prevention [4].
Conclusions
This survey of national policies on antimicrobial use in
food animal production demonstrates that multiple juris-
dictions have adopted mandatory restrictions on anti-
microbial use while the U.S. has slowly pursued a
voluntary approach to this issue [4]. The experiences of
Denmark and Sweden suggest that such restrictions may
be adopted with minimal economic repercussions for food
animal producers. Notably, the economic consequences of
permitting antimicrobial use for growth promotion and
disease prevention may be substantial given the import-
ance of export markets to the U.S. food animal industry
and the potential for trade barriers based on differences in
antimicrobial use. To preserve the efficacy of antimicro-
bial drugs for treatment of infections in humans and other
animals, the available scientific evidence indicates that the
U.S. should restrict antimicrobial use [7,8,17]. The poten-
tial economic consequences of waiting to align antimicro-
bial use policies with those of current and potential export
markets strengthens this case.
Endnotes
a
The magazine Bloomberg Businessweek reported that
the World Organization for Animal Health (better
known by its French acronym, OIE) had estimated that
the EU’s ban on antimicrobial growth promoters “re-
duced productivity for livestock breeders in the 27-
nation bloc by about 5 percent compared with the rest
of the world.”We were unable to locate a source for this
report online, and multiple emails to the reporter and, in
one case, the responsible editor went unanswered.
Competing interests
The authors declare that they have no competing interests.
Authors’contributions
DFM contributed to study design, led data collection and analysis, and led
the drafting of the manuscript. TJS originated the study, contributed to study
design, participated in data analysis, and drafted sections of the manuscript.
KEN contributed to study design, participated in data analysis, contributed to
revisions, and provided expertise and oversight. All authors read and
approved the final manuscript.
Maron et al. Globalization and Health 2013, 9:48 Page 9 of 11
http://www.globalizationandhealth.com/content/9/1/48
Acknowledgments
Thank you to Kate Clancy, Meghan Davis, Bob Lawrence, and Shawn
McKenzie for their careful review and thoughtful feedback on the
manuscript, and to Bill Weida for assistance with economic principles. Thank
you to individuals who provided information on antimicrobial use policies
included above. At the time of writing, DFM was based at the Johns Hopkins
Center for a Livable Future, which supported this research.
Author details
1
Johns Hopkins Center for a Livable Future, Johns Hopkins University, 615 North
Wolfe Street, Suite W7010, Baltimore, MD 21205, USA.
2
Department of
Environmental Health Sciences, Bloomberg School of Public Health, Johns
Hopkins University, 615 North Wolfe Street, Baltimore, MD 21205, USA.
3
Department of Health Policy and Management, Bloomberg School of Public
Health, Johns Hopkins University, 624 North Broadway, Baltimore, MD 21205, USA.
Received: 3 May 2013 Accepted: 23 August 2013
Published: 16 October 2013
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doi:10.1186/1744-8603-9-48
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survey. Globalization and Health 2013 9:48.
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