Abstract

Use of antibiotics as growth promoters in animal feeds has been permitted in the member states of the European Union during the last 50 yr. However, concerns about development of antimicrobial resistance and about transference of antibiotic resistance genes from animal to human microbiota, led to withdraw approval for antibiotics as growth promoters in the European Union since January 1, 2006. This report analyzes the history of European legislation regarding the use of antibiotics in poultry feeds, since the first harmonization by Directive 70/524 until Regulation 1831/2003 deleted these substances from the European Register of additives permitted in feeds. The European support to recommendations of the World Health Organization, the Food and Agriculture Organization, and the World Organization for Animal Health for a ban on antimicrobial use in animal feeds is expected to favor other countries also phase these substances out.

INTRODUCTION

The growth promoter effect of antibiotics was discovered in the 1940s, when it was observed that animals fed dried mycelia of Streptomyces aureofaciens containing chlortetracycline residues improved their growth. The mechanism of action of antibiotics as growth promoters is related to interactions with intestinal microbial population (Dibner and Richards, 2005; Niewold, 2007).

The United States Food and Drug Administration approved the use of antibiotics as animal additives without veterinary prescription in 1951 (Jones and Ricke, 2003). Also in the 1950s and 1960s, each European state approved its own national regulations about the use of antibiotics in animal feeds.

European Regulation Concerning Additives in Animal Feeds

European harmonization of regulations concerning additives in feedingstuffs aimed the establishment and functioning of the common market for animal feeds, since national regulations of each member state differed as regards to their basic principles. Council Directive 70/524, published in the Official Journal L 270 of December 14, 1970, underlaid the basis principle of regulation: only those additives which are named in this Directive may be contained in feedingstuffs and only subject to the requirements set out herein.

The member states, within 2 yr following notification, brought into force the laws, regulations, and administrative provisions necessary to comply with this Directive, and from November 25, 1972, additives, feedingstuffs containing additives and human foods from livestock fed additives were subject only to the marketing restrictions provided for in this Directive. This regulation also applied to other countries of the European Economic Area (Ice-land, Norway).

Recently, Directive 70/524 was replaced by Regulation 1831/2003 of the European Parliament and of the Council on additives for use in animal nutrition. Regulation 1831/ 2003 stated that antibiotics, other than coccidiostats and histomonostats, might be marketed and used as feed additives only until December 31, 2005. Anticoccidial substances, such as antibiotics ionophores, also will be prohibited as feed additives before 2013. After this date, medical substances in animal feeds will be limited to therapeutic use by veterinary prescription. European legislation can be consulted in http://eur-lex.europa.eu/en/index.htm

National Authorization Vs. European Authorization

Antibiotics permitted in the European feeds were listed in the annexes to Directive 70/524: annex I listed antibiotics without marketing restrictions in all the European Community, and annex II listed antibiotic that could be allowed by a state within its territory. When the use of certain additives authorized at national level had been widely tested, and the studies carried out and the experience gained indicated that these additives might be authorized throughout the Community for the uses specified, those additives were included in annex I. Annex II constituted therefore an intermediate stage in determining the inclusion of additives in the list of those permitted in the Community listed in the annex I. Annexes to Directive 70/524 were regularly amended in the light of scientific and technical knowledge.

ANTIBIOTIC ADDITIVES THAT WERE PERMITTED IN POULTRY FEEDS

The antibiotics which were authorized to be included in poultry feeds without a veterinary prescription are shown in Tables 11 and 22. Moreover, until December 3, 1986 (Directive 84/587) two authorized antibiotics could be mixed if they did not belong to the same chemical group.

Antibiotics That Were Authorized Only at the National Level

Annex II to Directive 70/524 listed the following antibiotics: bacitracin manganese, neomycin, soframycin (or framicetin), hygromycin-B, tylosin, and erythromycin. These antibiotics could be permitted at national scale with the conditions stated by each state. However, Directive 76/296 withdrew approval for these products after June 30, 1976 (December 31, 1976 for hygromycin-B), except the use of erithromycine in feeds for fattening chicks, which was extended until the end of 1978 by Directive 78/58.

Other antibiotics which were later added to annex II to be used in feeds for poultry (excluding ducks, geese, and laying hens) up to 10 wk old were lincomycin (Directive 74/180, authorized until June 30, 1981) and bacitracin-methylene-disalicylate (Directive 75/267, until December 31, 1977). Also the following antibiotics were included in annex II to be used only in feeds for chickens for fattening: mocimycin (Directive 78/743, until November 30, 1983), nosiheptide (Directive 79/1011, until December 3, 1986) and ardacin (Directive 94/77, until November 30, 1997).

Antibiotics Listed in Annex I to Directive 70/524

Annex I to Directive 70/524 listed the additives permitted in feeds to be marketed in the Community: Member states could not restrict the marketing of the feeds containing these additives. The antibiotics initially listed in annex I to be included in poultry feeds (excluding ducks, geese, and laying hens) were tetracyclines (tetracycline, chlortetracycline, and oxytetracycline) and penicillins (penicillin-G-potassium, penicillin-G-sodium, and penicillin-G-procaine) in feeds for poultry up to 10 wk old. Also oleandomycin, spiramycin, virginiamycin, bacitracin zinc, and flavophospholipol were permitted in feeds for poultry up to 10 wk old, raised up to 16 wk (26 wk for turkey) by Directive 76/13. Bacitracin zinc was also permitted by Directive 75/267 in feeds for ducks at national level until the end 1978.

Later, virginiamycin, bacitracin zinc, and flavophospholipol were approved for use also in feeds for laying hens, at first at a national scale (Directives 83/266, 74/ 180, and 78/974, respectively) and finally they were included in annex I by Directive 88/616 (virginiamycin) and Directive 78/974 (bacitracin zinc and flavophospholipol).

Other antibiotics added to annexes to Directive 70/ 524 to be included in poultry feeds were avoparcin and avilamycin. These products were authorized in feeds for chickens for fattening, at first at the national level (Directives 76/603 and 90/412, respectively) and finally included in annex I by Directives 79/1011 and 95/37, respectively. These products were also permitted in feeds for turkeys for fattening: ardacin was included in annex I by Directive 82/91, and avilamycin was permitted by Directive 97/72 at a national scale until November 30, 1998.

THE EUROPEAN BANS OF ANTIBIOTICS

The risk concerning residues of antibiotics in edible tissues and products that can produce allergic or toxic reactions in consumers is known to be negligible (Donoghue, 2003) because only antibiotics that are not absorbed in the digestive tract are authorized as growth promoters. However, the wider use of antibiotics as feed additives in the long run can contribute to the development of resistant bacteria to drugs used to treat infections. These microbials with resistant genes poses a potential risk for humans if they are transferred to persons. For this reason, the World Health Organization (1997) and the Economic and Social Committee of the European Union (1998) concluded that the use of antimicrobials in food animals is a public health issue.

The Former Bans

As soon as the 1970s, antibiotics from classes which were or might be used in human or veterinary medicine were transferred from annex I to annex II to phase them out after a certain period. It was the case of tetracyclines (Directive 73/264), penicillins (Directive 73/275), and oleandomycin (Directive 78/743), which were placed in annex II to be used only at a national scale in feeds for poultry. This national authorization was limited until June 30, 1976 (tetracyclines and penicillins) or September 30, 1979 (oleandomycin).

The Bans Proposed by Member States and the Sweden Case

A member state which, as a result of new information or of a reassessment of existing information made since the provisions in question were adopted, had detailed grounds for establishing that the use of one of the additives authorized at the Community scale constituted a danger to animal or human health or the environment could temporarily suspend the authorization to use that additive in its territory, and it should forthwith inform the Commission; member states should not, however, be able to have recourse to that power to hinder the free movement of the products. According the information provided by the state, a decision on the additive was taken.

Sweden prohibited in 1986 the use in feedingstuffs of additives belonging to the groups of antibiotics. When Sweden accessed in 1995 as a member of the European Union, it was authorized to maintain in force until December 31, 1998, its legislation before accession. Before that date, Sweden submitted applications, accompanied by detailed scientific grounds, for adjustments for the antibiotics authorized in the Community.

Also, other member states prohibited on their territories the use of some antibiotics in animal feedstuffs. Avoparcin was banned in Denmark (May 20, 1995) and Germany (January 19, 1996) arguing that this glycopeptide antibiotic produces resistance to glycopeptides used in human medicine, spiramycin was prohibited in Finland (January 1, 1998) because this product was used in human medicine, and virginiamycin was prohibited in Denmark (January 15, 1998) because 2 streptogramins were clinically important in human medicine.

As results of this national initiatives, Directive 97/6 withdrew approval for Avoparcin from 1 April 1997, and Regulation 2821/1998 banned spiramycin and virginiamycin from June 30, 1999. Regulation 2821/1998 also banned bacitracin zinc because its use in human medicine as treatment of infections of the skin.

The Last Ban

On January 1, 1999, Sweden applied the safeguard clause for the antibiotics still authorized as feed additives, including those still permitted in poultry feeds: flavophospholipol and avilamycin. The scientific ground submitted by Sweden, as well as the conclusions of the World Health Organization (1997) and of the Economic and Social Committee of the European Union (1998), led to no longer to authorize the use of antibiotics as growth promoters: Regulation 1831/2003 stated that antibiotics, other than coccidiostats and histomonostats, might be marketed and used as feed additives only until December 31, 2005; as from January 1, 2006, those substances would be deleted from the Community Register of authorized feed additives.

EXPECTED CONSEQUENCES OF THE BAN

The main expected consequence of the ban is a reduction of the amount of antibiotics used in animal production, and therefore the risk of transferring to persons of microbials with resistant genes to antibiotics. Available data suggest that the growth-promoter ban has driven an increase in infections and therefore a substantial increase in the use of therapeutic antibiotics for food animals in Europe, but the ban also has reduced overall antibiotic use in animals (Casewell et al., 2003). Wierup (2001) also reported that in Sweden, as a result of the ban and a focus on disease prevention and correct use of antimicrobials, the total use of antibacterial drugs to animals decreased by approximately 55% in the period 1986–1999, and a relatively low prevalence of antimicrobial resistance has been maintained.

In other ways, the ban of growth promoters demands the improvement of the hygiene of farms. It was shown that under good production conditions it is possible to reach good and competitive production results for the rearing of poultry without the continuous use of antibiotics in feeds (Wierup, 2001; Engster et al., 2002; World Health Organization, 2002). Moreover, safer nonantimicrobial substances have been studied as alternatives for replacing antibiotics to interact with the intestinal microflora, including enzymes (Bedford, 2000; Hruby and Cowieson, 2006), prebiotics, and probiotics (Patterson and Burkholder, 2003; Kocher, 2006), or acidification of diets (Ricke, 2003; Diebold and Eidelsburger, 2006).

Finally, the ban of antibiotics in animal feeds will have consequences in the international trade of poultry meat because the European Union only imports foods obtained from animals that were not fed with antibiotics, in application of the precaution principle allowed by the World Trade Organization. However, because concern is rising that drug-resistant pathogens could be transmitted to humans via the food-chain (World Health Organization, 2003, 2004), it is expected that the use of antimicrobials in animal production will decrease in further years, at least in those farms with better hygiene conditions.

Table 1.

Antibiotics which were permitted as feed additives only in national poultry feeds

Antibiotic Species of animal Maximum content of additive in complete feeds and period of authorization Legislative references 
Bacitracin manganese, Neomycin, tylosin, soframycin Only national restrictions November 25, 1970 to June 30, 1976 Directives 70/524, 75/296 
Hygromycin-B Only national restrictions November 25, 1970 to December 31, 1976 Directives 70/524, 75/296, 76/603 
Erythromycin Only national restrictions
 Chickens for fattening November 25, 1970 to June 23, 1976
 20 ppm, June 24, 1976 to December 31, 1978 Directives 70/524, 75/296, 76/603
 Directives 76/603, 78/58 
Bacitracin-methylene-disalicylate Poultry (excluding ducks, geese, and laying hens) up to 10 wk old 20 ppm, April 29, 1975 to December 31, 1977 Directives 75/267, 75/296, 76/603 
Lincomycine Poultry (excluding ducks, geese, and laying hens) up to 10 wk old 10 ppm, March 5, 1974 to June 30, 1981 Directives 74/180, 75/296, 76/603, 78/58, 79/139, 79/553, 80/618, 80/1139 
Mocimycin Chickens for fattening 5 ppm, August 1, 1978 to November 30, 1983 Directives 78/743, 80/1156, 82/91, 82/822 
Nosiheptide Chickens for fattening 10 ppm, November 16, 1979 to December 3, 1986 Directives 79/1011, 80/1156, 82/91, 82/822, 83/466, 84/349, 85/342, 85/520 
Ardacin Chickens for fattening 7 ppm, January 20, 1995 to November 30, 1997 Directives 94/77, 95/55, 96/66, 97/72 
Antibiotic Species of animal Maximum content of additive in complete feeds and period of authorization Legislative references 
Bacitracin manganese, Neomycin, tylosin, soframycin Only national restrictions November 25, 1970 to June 30, 1976 Directives 70/524, 75/296 
Hygromycin-B Only national restrictions November 25, 1970 to December 31, 1976 Directives 70/524, 75/296, 76/603 
Erythromycin Only national restrictions
 Chickens for fattening November 25, 1970 to June 23, 1976
 20 ppm, June 24, 1976 to December 31, 1978 Directives 70/524, 75/296, 76/603
 Directives 76/603, 78/58 
Bacitracin-methylene-disalicylate Poultry (excluding ducks, geese, and laying hens) up to 10 wk old 20 ppm, April 29, 1975 to December 31, 1977 Directives 75/267, 75/296, 76/603 
Lincomycine Poultry (excluding ducks, geese, and laying hens) up to 10 wk old 10 ppm, March 5, 1974 to June 30, 1981 Directives 74/180, 75/296, 76/603, 78/58, 79/139, 79/553, 80/618, 80/1139 
Mocimycin Chickens for fattening 5 ppm, August 1, 1978 to November 30, 1983 Directives 78/743, 80/1156, 82/91, 82/822 
Nosiheptide Chickens for fattening 10 ppm, November 16, 1979 to December 3, 1986 Directives 79/1011, 80/1156, 82/91, 82/822, 83/466, 84/349, 85/342, 85/520 
Ardacin Chickens for fattening 7 ppm, January 20, 1995 to November 30, 1997 Directives 94/77, 95/55, 96/66, 97/72 
Table 2.

Antibiotics that were permitted as feed additives in poultry feeds for the Community market

Antibiotic Species of animal Maximum content of additive in complete feeds and period of national authorization Maximum content of additive in complete feeds and period of Community authorization Legislative references 
Tetracycline, chlortetracycline, oxytetracycline Poultry (except ducks, geese, laying hens) up to 10 wk old 20 ppm (50 ppm up to 4 wk)
 November 25, 1970 to June 30, 1976 20 ppm, November 25, 1972 to August 5, 1973 Directives 70/524, 73/264, 75/296 
Penicillin-G-potassium, penicillin- G-sodium, penicillin-G-procain Poultry (except ducks, geese, laying hens) up to 10 wk old 20 ppm (50 ppm up to 4 wk)
 November 25, 1970 to June 30, 1976 20 ppm, November 25, 1972 to August 5, 1973 Directives 70/524, 73/275, 75/296 
Oleandomycin Poultry (except ducks, geese, laying hens) up to 4 wk old
 
 Poultry (except ducks, geese, laying hens) between 5 and 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, laying hens, pigeons) between 11 and 16 wk old
 Turkeys for fattening up to 16 wk old 25 ppm, November 25, 1970 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979 10 ppm (25 ppm up to 4 wk), November 25, 1970 to March 31, 1976 20 ppm (25 ppm up to 4 wk), April 1, 1976 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979
 20 ppm, December 18, 1975 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979
 
 20 ppm, February 4, 1982 to April 1, 1997 10 ppm, November 25, 1972 to March 31, 1976 20 ppm, April 1, 1976 to July 31, 1978
 
 20 ppm, July 1, 1982 to February 7, 1997 Directives 70/524, 76/13, 76/603, 78/58, 78/743 
Spiramycin Poultry (except ducks, geese, laying hens) up to 4 wk old
 Poultry (except ducks, geese, pigeons, and laying hens) between 5 and 10 wk old
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, laying hens, pigeons) between 11 and 16 wk old 50 ppm, November 25, 1970 to December 31, 1978
 20 ppm, January 1, 1979 to June 30, 1999
 20 ppm, November 25, 1970 to June 30, 1999
 20 ppm, December 18, 1975 to June 30, 1999 20 ppm, November 25, 1972 to December 28, 1998
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 76/13, 76/603, 78/58, 80/678, Regulation 2821/98 
Virginiamycin Laying hens
 
 Other poultry (except ducks, geese) up to 4 wk old
 
 Other poultry (except ducks, geese) between 5 and 10 wk old
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 20 ppm, May 17, 1983 to June 30, 1999
 
 20 ppm, November 25, 1970 to May 3, 1973
 50 ppm, May 4, 1973 to December 31, 1978
 20 ppm, January 1, 1979 to June 30, 1999
 20 ppm, November 25, 1970 to June 30, 1999
 20 ppm, December 18, 1975 to June 30, 1999 20 ppm, June 30, 1989 to December 28, 1998
 
 20 ppm, November 25, 1972 to December 28, 1998
 
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 73/103, 76/13, 76/603, 78/58, 83/266, 85/520, 86/403, 87/552, 88/616, Regulation 2821/98 
Bacitracin zinc Laying hens
 
 Ducks up to 10 wk old
 Other poultry (except ducks, geese, pigeons) up to 4 wk old
 Other poultry (except ducks, geese, pigeons) between 5 and 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 20 ppm (100 ppm since December 18, 1975), March 5, 1974 to June 30, 1999
 
 10 ppm, April 29, 1975 to December 31, 1978
 50 ppm, November 25, 1970 to June 30, 1999
 
 20 ppm, November 25, 1970 to June 30, 1999
 Chickens for fattening: 50 ppm, September 1, 1994 to November 30, 1998
 20 ppm, December 18, 1975 to June 30, 1999
 Chickens for fattening: 50 ppm, September 1, 1994 to November 30, 1998 100 ppm, June 30, 1979 to December 28, 1998
 
 Not permitted
 50 ppm, December 31, 1978 to December 28, 1998
 20 ppm, November 25, 1972 to December 28, 1998
 
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 74/180, 75/267, 75/296, 76/13, 76/603, 77/471, 78/58, 78/743, 78/974, 94/41, 95/55, 96/66, 97/72, Regulation 2821/98 
Antibiotic Species of animal Maximum content of additive in complete feeds and period of national authorization Maximum content of additive in complete feeds and period of Community authorization Legislative references 
Tetracycline, chlortetracycline, oxytetracycline Poultry (except ducks, geese, laying hens) up to 10 wk old 20 ppm (50 ppm up to 4 wk)
 November 25, 1970 to June 30, 1976 20 ppm, November 25, 1972 to August 5, 1973 Directives 70/524, 73/264, 75/296 
Penicillin-G-potassium, penicillin- G-sodium, penicillin-G-procain Poultry (except ducks, geese, laying hens) up to 10 wk old 20 ppm (50 ppm up to 4 wk)
 November 25, 1970 to June 30, 1976 20 ppm, November 25, 1972 to August 5, 1973 Directives 70/524, 73/275, 75/296 
Oleandomycin Poultry (except ducks, geese, laying hens) up to 4 wk old
 
 Poultry (except ducks, geese, laying hens) between 5 and 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, laying hens, pigeons) between 11 and 16 wk old
 Turkeys for fattening up to 16 wk old 25 ppm, November 25, 1970 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979 10 ppm (25 ppm up to 4 wk), November 25, 1970 to March 31, 1976 20 ppm (25 ppm up to 4 wk), April 1, 1976 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979
 20 ppm, December 18, 1975 to July 31, 1978 10 ppm, August 1, 1978 to September 30, 1979
 
 20 ppm, February 4, 1982 to April 1, 1997 10 ppm, November 25, 1972 to March 31, 1976 20 ppm, April 1, 1976 to July 31, 1978
 
 20 ppm, July 1, 1982 to February 7, 1997 Directives 70/524, 76/13, 76/603, 78/58, 78/743 
Spiramycin Poultry (except ducks, geese, laying hens) up to 4 wk old
 Poultry (except ducks, geese, pigeons, and laying hens) between 5 and 10 wk old
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, laying hens, pigeons) between 11 and 16 wk old 50 ppm, November 25, 1970 to December 31, 1978
 20 ppm, January 1, 1979 to June 30, 1999
 20 ppm, November 25, 1970 to June 30, 1999
 20 ppm, December 18, 1975 to June 30, 1999 20 ppm, November 25, 1972 to December 28, 1998
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 76/13, 76/603, 78/58, 80/678, Regulation 2821/98 
Virginiamycin Laying hens
 
 Other poultry (except ducks, geese) up to 4 wk old
 
 Other poultry (except ducks, geese) between 5 and 10 wk old
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 20 ppm, May 17, 1983 to June 30, 1999
 
 20 ppm, November 25, 1970 to May 3, 1973
 50 ppm, May 4, 1973 to December 31, 1978
 20 ppm, January 1, 1979 to June 30, 1999
 20 ppm, November 25, 1970 to June 30, 1999
 20 ppm, December 18, 1975 to June 30, 1999 20 ppm, June 30, 1989 to December 28, 1998
 
 20 ppm, November 25, 1972 to December 28, 1998
 
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 73/103, 76/13, 76/603, 78/58, 83/266, 85/520, 86/403, 87/552, 88/616, Regulation 2821/98 
Bacitracin zinc Laying hens
 
 Ducks up to 10 wk old
 Other poultry (except ducks, geese, pigeons) up to 4 wk old
 Other poultry (except ducks, geese, pigeons) between 5 and 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 20 ppm (100 ppm since December 18, 1975), March 5, 1974 to June 30, 1999
 
 10 ppm, April 29, 1975 to December 31, 1978
 50 ppm, November 25, 1970 to June 30, 1999
 
 20 ppm, November 25, 1970 to June 30, 1999
 Chickens for fattening: 50 ppm, September 1, 1994 to November 30, 1998
 20 ppm, December 18, 1975 to June 30, 1999
 Chickens for fattening: 50 ppm, September 1, 1994 to November 30, 1998 100 ppm, June 30, 1979 to December 28, 1998
 
 Not permitted
 50 ppm, December 31, 1978 to December 28, 1998
 20 ppm, November 25, 1972 to December 28, 1998
 
 20 ppm, April 1, 1976 to December 28, 1998 Directives 70/524, 74/180, 75/267, 75/296, 76/13, 76/603, 77/471, 78/58, 78/743, 78/974, 94/41, 95/55, 96/66, 97/72, Regulation 2821/98 
Flavophospholipol Laying hens
 
 Chickens for fattening up to 10 wk old
 
 Chickens for fattening between 11 and 16 wk old
 
 Other poultry (except ducks, geese) up to 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 5 ppm, March 5, 1974 to December 31, 2005
 
 20 ppm, November 25, 1970 to December 31, 2005
 
 20 ppm, December 18, 1975 to December 31, 2005
 
 20 ppm, November 25, 1970 to May 15, 2002
 
 20 ppm, December 18, 1975 to May 15, 2002 5 ppm, June 30, 1979 to December 31, 2005
 
 20 ppm, November 25, 1972 to December 31, 2005
 20 ppm, April 1, 1976 to December 31, 2005
 20 ppm, November 25, 1972 to May 15, 2002
 20 ppm, April 1, 1976 to May 15, 2002 Directives 70/524, 74/180, 75/296, 76/13, 77/471, 78/58, 78/974, Regulations 2205/01, 1831/03 
Avilamycin Chickens for fattening
 Turkeys 10 ppm, July 23, 1990 to December 31, 2005
 
 10 ppm, January 12, 1997 to November 30, 1998 10 ppm, June 30, 1996 to December 31, 2005
 
 Not permitted Directives 90/412, 91/620, 92/99, 93/107, 94/50, 95/37, 97/72, Regulation 1831/05 
Avoparcin Chickens for fattening
 
 Turkeys for fattening up to 16 wk old 15 ppm, June 24, 1976 to April 1, 1997
 
 20 ppm, February 4, 1982 to April 1, 1997 15 ppm, January 1, 1980 to February 7, 1997
 20 ppm, July 1, 1982 to February 7, 1997 Directives 76/603, 78/58, 78/974, 79/697, 79/1011, 82/91, 97/6 
Flavophospholipol Laying hens
 
 Chickens for fattening up to 10 wk old
 
 Chickens for fattening between 11 and 16 wk old
 
 Other poultry (except ducks, geese) up to 10 wk old
 
 Turkeys between 11 and 26 wk old, and other poultry (except ducks, geese, pigeons) between 11 and 16 wk old 5 ppm, March 5, 1974 to December 31, 2005
 
 20 ppm, November 25, 1970 to December 31, 2005
 
 20 ppm, December 18, 1975 to December 31, 2005
 
 20 ppm, November 25, 1970 to May 15, 2002
 
 20 ppm, December 18, 1975 to May 15, 2002 5 ppm, June 30, 1979 to December 31, 2005
 
 20 ppm, November 25, 1972 to December 31, 2005
 20 ppm, April 1, 1976 to December 31, 2005
 20 ppm, November 25, 1972 to May 15, 2002
 20 ppm, April 1, 1976 to May 15, 2002 Directives 70/524, 74/180, 75/296, 76/13, 77/471, 78/58, 78/974, Regulations 2205/01, 1831/03 
Avilamycin Chickens for fattening
 Turkeys 10 ppm, July 23, 1990 to December 31, 2005
 
 10 ppm, January 12, 1997 to November 30, 1998 10 ppm, June 30, 1996 to December 31, 2005
 
 Not permitted Directives 90/412, 91/620, 92/99, 93/107, 94/50, 95/37, 97/72, Regulation 1831/05 
Avoparcin Chickens for fattening
 
 Turkeys for fattening up to 16 wk old 15 ppm, June 24, 1976 to April 1, 1997
 
 20 ppm, February 4, 1982 to April 1, 1997 15 ppm, January 1, 1980 to February 7, 1997
 20 ppm, July 1, 1982 to February 7, 1997 Directives 76/603, 78/58, 78/974, 79/697, 79/1011, 82/91, 97/6 

REFERENCES

Bedford
,
M.
2000
. Removal of antibiotic growth promoters from poultry diets: Implications and strategies to minimise subsequent problems.
World’s Poult. Sci. J.
 
56
:
347
–365.
Casewell
,
M.
, C. Friis, E. Marco, P. McMullin, and I. Phillips.
2003
. The European ban on growth-promoting antibiotics and emerging consequences for human and animal health.
J. Antimicrob. Chemother.
 
52
:
159
–161.
Dibner
,
J. J.
, and J. D. Richards.
2005
. Antibiotic growth promoters in agriculture: History and mode of action.
Poult. Sci.
 
84
:
634
–643.
Diebold
,
G.
, and U. Eidelsburger.
2006
. Acidification of diets as an alternative to antibiotic growth promoters. Pages 311–327 in Antimicrobial Growth Promoters: Where Do We Go From Here? D. Barug, J. de Long, A. K. Kies, and M. W. A. Verstegen, ed. Wageningen Acad. Publ., Wageningen, the Netherlands.
Donoghue
,
D. J.
2003
. Antibiotic residues in poultry tissues and eggs: Human health concerns?
Poult. Sci.
 
82
:
618
–621.
Economic and Social Committee of the European Union.
1998
. Opinion on resistance to antibiotics as a threat to public health. No. ESC-98-016-EN. http://eescopinions.eesc.europa.eu/EESCopinionDocument.aspx?identifier=ces\anciennes_sections\envi\envi471\ces1118-1998_ac.doc&language=EN Accessed Jun. 2007.
Engster
,
H. M.
, D. Marvil, and B. Stewart-Brown.
2002
. The effect of withdrawing growth promoting antibiotics from broiler chickens: A long-term commercial industry study.
J. Appl. Poult. Res.
 
11
:
431
–436.
Hruby
,
M.
, and A. J. Cowieson. A. J.
2006
. The role of enzymes and betaine in antibiotic growth promoter free nutrition. Pages 269–287 in Antimicrobial Growth Promoters: Where Do We Go From Here? D. Barug, J. de Long, A. K. Kies, and M. W. A. Verstegen, ed. Wageningen Acad. Publ., Wageningen, the Netherlands.
Jones
,
F. T.
, and S. C. Ricke.
2003
. Observations on the history of the development of antimicrobials and their use in poultry feeds.
Poult. Sci.
 
82
:
613
–617.
Kocher
,
A.
2006
. Interfacing gut health and nutrition: The use of dietary prebiotics and probiotics to maximise growth performance in pigs and poultry. Pages 289–310 in Antimicrobial Growth Promoters: Where Do We Go From Here? D. Barug, J. de Long, A. K. Kies, and M. W. A. Verstegen, ed. Wageningen Acad. Publ., Wageningen, the Netherlands.
Niewold
,
T. A.
2007
. The nonantibiotic antiinflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis.
Poult. Sci.
 
86
:
605
–609.
Patterson
,
J. A.
, and K. M. Burkholder.
2003
. Application of prebiotics and probiotics in poultry production.
Poult. Sci.
 
82
:
627
–631.
Ricke
,
S. C.
2003
. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials.
Poult. Sci.
 
82
:
632
–639.
Wierup
,
M.
2001
. The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials.
Microb. Drug Resist.
 
7
:
183
–190.
World Health Organization.
1997
. The medical impact of the use of antimicrobials in food animals: Report of a WHO meeting, Berlin, Germany. http://whqlibdoc.who.int/hq/1997/WHO_EMC_ZOO_97.4.pdf Accessed Jun. 2007.
World Health Organization.
2002
. Impacts of antimicrobial growth promoter termination in Denmark. Foulum, Denmark. http://www.who.int/salmsurv/en/Expertsreportgrowthpromoterdenmark.pdf Accessed Jun. 2007.
World Health Organization.
2003
. First joint FAO/OIE/WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: Scientific assessment. Geneva, Switzerland. http://whqlibdoc.who.int/hq/2004/WHO_CDS_CPE_ZFK_2004.7.pdf Accessed Jun. 2007.
World Health Organization.
2004
. Second joint FAO/OIE/ WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: Management options. Oslo, Norway. http://whqlibdoc.who.int/hq/2004/WHO_CDS_CPE_ZFK_2004.8.pdf Accessed Jun. 2007.