European Union

EU-wide, limitations on antimicrobial use began in 1997 when the EU banned using avoparcin for growth promotion [27]. In 1999, the bloc also banned growth promotion uses of tylosin, spiramycin, bacitracin, virginiamycin, carbadox, and olaquindox [27]. Remaining growth promotion uses were banned in 2006 [27]. Although the EU requires veterinary prescriptions to use antimicrobials in food animals, it allows member states to grant exemptions in certain cases. EU-wide information on the full economic 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 commodities (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 available in English for us to verify. Taiwan accounts for approximately 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 monitoring AMR in food and animal pathogens through its MARAN system [28]. Using MARAN data, it was reported that total sales of antibiotics licensed for therapeutic use in the Netherlands declined by nearly 32% (from 495 to 338 tonnes) between 2009 and 2011, surpassing 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 identify separate regulations pertaining to prophylactic antimicrobial 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 prescriptions are required to administer antimicrobials.

In 2008, Germany enacted its own national antibiotic resistance strategy, Deutsche Antibiotika-Resistenzstrategie or “DART”. That strategy includes AMR monitoring, improved data-sharing on resistance issues, and reducing antibiotic use through better environmental prevention of infectious diseases [32]. German state governments are responsible 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 prescribed by veterinarians and the quantities actually consumed by food animals. Germany will also collect data on pharmaceutical use by the poultry industry for the first time. As a result of these provisions, the government expects to be able to track pharmaceutical use to individual 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 national 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 measures to limit antimicrobial use. In 2002, Denmark prohibited veterinarians from using fluoroquinolones except in cases where antimicrobial susceptibility testing of clinical isolates indicated that no other antibiotic could render 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 immediately 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, production 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 production impacts from the ban on AGPs, apart from a small increase in the feed-conversion ratio [39]. Danish industry representatives now report that changes to their production practices, such as later weaning, improved diet, and lower stocking densities, minimized negative impacts [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 animal 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 infections. 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 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 therapeutic 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 results 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 slaughter 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 kilograms, 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 obtain 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).

Mexico

In 2007, Mexico enacted its Federal Law of Animal Health, which restricts AGP use in animal feed and requires a veterinary 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. Antimicrobial disease prevention and control regulations were unavailable in English. Mexico is the number one destination point for U.S. food animal product exports, responsible for 17.1 percent of U.S. export sales of those products annually (Table 2).

Japan

Japan does not have any restrictions on using antimicrobials for growth promotion, but its Food Safety Commission is reportedly considering restricting some uses of antibiotics. A veterinary prescription is required for antimicrobial 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 restricts AGPs or requires a veterinary prescription to use antimicrobials. In July 2010, however, South Korea announced a ban on the “addition of antibiotics in animal feed…to strengthen the safety management of domestic livestock products” [22]. This ban, geared toward limiting the amount of drugs added into premixed 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 oversight [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 expected no earlier than 2012, although we could not determine 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 products 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 prescription 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 antimicrobial 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).

Philippines

We could not determine current policies in the Philippines related to restrictions on antimicrobial use in food animals or veterinarian prescription requirements. Efforts to communicate with Philippines officials were unsuccessful. The Philippines are responsible for 2.2% of annual U.S. food animal product export sales (Table 2).