HAL Id: hal-00889716https://hal.archives-ouvertes.fr/hal-00889716

Submitted on 1 Jan 1998

HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.

Growth promotants in feeding pigs and poultry. I.Growth and feed efficiency responses to antibiotic

growth promotantsSigvard Thomke, Klas Elwinger

To cite this version:Sigvard Thomke, Klas Elwinger. Growth promotants in feeding pigs and poultry. I. Growth and feedefficiency responses to antibiotic growth promotants. Annales de zootechnie, INRA/EDP Sciences,1998, 47 (2), pp.85-97. �hal-00889716�

Review

Growth promotants in feeding pigs and poultry.I. Growth and feed efficiency responses

to antibiotic growth promotants

Sigvard Thomke Klas Elwinger

Department of Animal Nutrition and Management, Sweden Univ. Agric. Science,P.O. Box 7024, S-750 07 Uppsala, Sweden

(Received 2 December 1997; accepted 5 January 1998)

Abstract - Since the beginning of the 1950s, growth promoters of antibiotic type have played amajor role in the development of intensive and industrialised animal farming systems. The incor-poration of such growth promoters into animal feed mixtures has made it possible to improve ani-mal health conditions as well as to increase rearing intensity. Simultaneously, the admixing of theseadditives has successively lowered food production costs, a development which has been to thebenefit of the consumer. The objective of this contribution was to review recent developments inthis area and in particular to address growth promoters of antibiotic type authorised in the Euro-pean Union as additives for pig and poultry. Finally, we also briefly touch upon the potential eco-nomic consequences of terminating their use under current European conditions, as well as theirpotential environmental effects. (© Elsevier / Inra)

growth promoter / antibiotic / pig / poultry

Résumé - Les promoteurs de croissance dans l’alimentation des porcs et des volailles.I. Réponses en terme de croissance et d’indice de consommation à l’addition d’antibio-tiques. Les promoteurs de croissance, tels les antibiotiques, ont joué un rôle important durant cesdernières décennies dans le développement des systèmes d’élevage intensif et industriel. Leur incor-poration dans l’alimentation animale a permis d’améliorer les conditions sanitaires des animauxet d’accroître la productivité des élevages, tout en diminuant simultanément les coûts de production.L’objectif de cet article est de passer en revue les connaissances nouvellement acquises dans cedomaine, et de s’intéresser plus particulièrement aux antibiotiques autorisés dans l’Union Euro-péenne et utilisés dans l’alimentation des porcs et des volailles. Sont également évoqués lesconséquences économiques de leur retrait dans le contexte européen actuel et leurs effets poten-tiels sur l’environnement. (© Elsevier / Inra)

promoteur de croissance / antibiotique / porc / volaille

* Correspondence and reprintsTel.: (46) 0 18 67 10 00; fax: (46) 0 l 8 67 29 95

1. INTRODUCTION

The general benefits of using antibioticgrowth promotants in livestock produc-tion are lower production costs leading tolower market prices and a more plentifulsupply of food commodities. For the con-sumer, the direct benefits are lowered food

prices [9]. However, there is growing con-cern among consumers in many countriesabout the use of growth promotants [2, 4,27, 30, 33]. The background for this con-cern is found in the risks for the occur-rence of residues of additives in animalfood products, the development of resis-tance of pathogenic microorganisms inanimals against antibiotic preparations,and the transfer of such germ plasma tohuman pathogenic microorganisms. Themore reluctant attitude prevailing in theUSA to a withdrawal of antibiotic pro-motants in livestock feeding is exempli-fied by the comprehensive review givenby DuPont and Steele [ I 1 i.

2. LIVESTOCK PRODUCTION

Livestock production is the result of anintegrated approach of selection, nutrition,housing and health care [16!. Over thecenturies there has been a gradualimprovement in the efficiency of livestockproduction. This development has accel-erated during recent decades by the intro-duction of more scientifically approvedmethods in the different areas of livestock

production and by continuously imple-menting research findings in practice. Sci-entific contributions in the fields of ani-mal physiology, genetics and nutrition aswell as veterinary sciences and housingengineering were of great importance forthe development of industrialized live-stock production systems. By these means,man’s ability to control and manipulateanimal production increased tremendouslyafter World War II. For the further devel-

opment of livestock production systems

in the future, one may expect the scien-tific fields of immunology and ethologyto become of increasing importance.

In the development of intensive andindustrialized livestock production dur-ing recent decades, antibiotic growth pro-motants, introduced in the early 1950s,have played a decisive role. Responses togrowth promotants, and hence return tothe farmer, will generally be maximizedby keeping target animals healthy and pro-viding them with adequate levels of nutri-ents and an appropriately balanced diet[30]. There is a variety of feed additiveswith growth promoting effects under dis-cussion and, according to Laming 1261,these can be categorized as follows:

- anabolic agents with the aim to alternutrient partitioning, i.e., to increase pro-tein deposition and yield of edible cuts;

- antimicrobial agents as to improvegrowth rate and feed efficiency and/or toprevent decreased growth rate in occur-rence of disease; probiotics and acidifiersmay be mentioned under this category;

- immunological methods to enhancegrowth rate or to improve carcass com-position;- (3-adrenergic agonists to modify car-

cass composition by altering nutrient par-titioning and lowering fat deposition,simultaneously increasing protein accre-tion.

Apart from these additives, a moredetailed understanding of the mechanismsin the hypothalamic-pituitary endocrinalcontrol of growth and metabolism could inthe future lead to other means of improve-ments in animal production processes.

The term growth promotant is used forfeed additives, other than dietary nutri-ents, which increase growth rate and/orimprove feed efficiency in healthy ani-mals, fed a balanced diet (Macgregor(1983) cited in [9]). According to the lit-erature review by De Craene and Viaene[9J and as mentioned in CEAS et al. [7],

there is a great variation in responses ofanimals to antibiotic growth promotantsaccording to different authors (table !.

Thus, one of the entries for growing-finishing pigs claims a response in growthrate of up to 20%, whereas for feed effi-ciency the lowest response was limited to0.7%. Furthermore, in judging these pro-moting effects one has to consider age andclass of animals and also the duration offeed additive administration as well as the

performance level of the control treatmentgroup. In comparing effects of admixing’antibiotic additives’ over time, one hasalso to consider the change from more

potent and medical preparations to othertypes, approved only as feed additives.The values by CEAS et al. [7] are obvi-ously regarded in the EU as useful for gen-eral calculations.

3. ANTIBIOTIC GROWTHPROMOTANTS IN USEIN THE EU

The antimicrobial preparations acteither bactericidally (e.g., penicillin) orbacteriostatically (e.g., tetracyclines).There is a third group of antimicrobial

additives, ionophores, which also controlprotozoal growth. These preparations areof particular interest as additives for rumi-nants and poultry.

The antibiotic growth promotantsapproved in the EU are listed in table II. Abrief description of their chemical andmicrobial properties is given by, e.g.,Hudd [23]. The approval of the individ-ual promotants is linked to minimum andmaximum levels of inclusion in the targetdiets. The level of supplementation of a

certain promotant may vary between ani-mal species and also between classes.Moreover, the levels of supplementationmay be regulated for the different stages ofdevelopment and to a maximum age ofanimals. The use of carbadox and olaquin-dox supplemented diets has to be discon-tinued not later than 4 weeks prior toslaughter. According to the potential ofthe additive, the dose of active ingredientmay vary between I and 100 ppm (mg perkg) in the target diet.

4. GROWTH AND FEEDEFFICIENCY RESPONSESTO PROMOTANTS IN PIGS

The main interest in exploiting antibi-otic growth promotants is in the sectorsof pig and poultry production [36]. Sincethe 1950s there has been a strong devel-

opment in the use of antibiotic promotants.The major part of the research in this areawith different animal species has been per-formed within the manufacturing and feedindustries, whereas a relatively limitedpart has been performed by independentresearch bodies [5].

Discrepancy exists concerning theeffect of antibiotic promotants on sow per-formance. Speer [44] concluded that thefarrowing rate was improved by the useof promotants. However, antibiotic pro-motants had no effects on oestrus, matingbehaviour or breeding efficiency [31 ]. Lit-ter weights at birth and at weaning wereimproved [42], which could not be cor-roborated by Fr6lich et al. [17] underSwedish conditions.

By testing different antibiotic growthpromotants in sows, Fr6lich et al. [17]found the number of resistant C. perfrin-gens strains in faecal samples to increaseby supplementation with aureomycin, ter-ramycin, oleandomycin or spiramycin,whereas such an increase was not observed

by supplementing Zn-bacitracin or vir-giniamycin.

The response of younger animals like

piglets (as well as broiler chickens andcalves) to promotants compared withunsupplemented diets is usually found tobe superior compared with adolescentclasses of these species. This is demon-strated for piglets, with growth responsesto promotants between 9 and 30% andfeed efficiency responses between 6 and12°70, whereas for growing-finishing pigsthe level of response is inferior (table III).The highest value given for piglets wasobtained by Nousiainen and Suomi [32] ]

by providing the promotant olaquindox ina water solution. These authors observeda significantly higher colonic digesta drymatter content in connection with pro-motant supplementation, which indicatesbetter health and also explains the higherfeed intake by the supplemented treatmentgroup.

The response to withdrawal of olaquin-dox from 1986 on piglet health and per-formance in 220 Swedish piglet producingherds was statistically evaluated byRobertsson and Lundeheim [34] by usingthe Swedish efficiency monitoring system(RASP). Removal of olaquindox from thepiglet diets was followed by a doublingof incidences of diarrhoea and number ofmedical treatments of diarrhoea post-weaning as well as by an increased mor-tality by about 1.5 percentage units. Onthe withdrawal of olaquindox as growthpromotant, the age at 25 kg increased by5-6 days. In recent years the AnimalHealth Service control programs have fur-ther been developed with guidelines forpracticing veterinarians and piglet pro-ducers, and measures have been taken toimprove management, animal environ-ment and feed composition, all of whichhave led to positive results in lowering theincidence or even preventing the occur-rence of diarrhoea [34].

In addition to the information given intable III, the report by Tarrago et al. [45]should be quoted as the supplementationof tylosin as well as of virginiamycinresulted in significant improvements inpiglet growth performance, but in non-significant improvement of feed effi-ciency.

This difference in responses between

piglets and growing-finishing pigs is fur-ther illustrated by a comprehensiveYugoslavian study [48]. These authorsinvestigated responses in piglets (6-20 kglive weight) fed diets supplemented witheither of four promotants and which werecompared with unsupplemented control

diets. One of these preparations, AureoSP-125, was the most potent and wasbased on therapeutically used antibiotics(see footnote in table III). Therefore, thefourth treatment was excluded. For the

remaining three promotants the growthresponses varied between 10 and 15% andthe feed efficiency responses between 5

and 10%a. Corresponding values for grow-ing-finishing pigs (20-90 kg) fed dietssupplemented with the same promotantsvaried between 5 and 8% (growth rate)and between 4 and 7% (feed efficiency),respectively.

Similarly, by comparing the promotanteffect of tylan on daily weight gains in the

growing phase with those in the finishingphase, Schneider [38] arrived at relativeresponses in growth rate of 4.7 and 2.4%,respectively. For feed efficiency, corre-sponding improvements were found to be9.1 and 2.8%, respectively. Lindermeyer etal. [29] also reported higher responses indaily weight gains and feed efficiency inthe growing phase (20-50 kg) of 13 and15°Io, respectively, versus 6 and 5% forthe entire growing-finishing period.

Responses by growing-finishing pigsto the feeding of growth-promoting agentsin the period from 1950 to 1984 were stud-ied by Gruber [19]. The most effectivegroup of growth promotants includedstreptomycin, penicillin and quinoxalines,whereas the least effective group included

taomycin, salinomycin, nitrovin and thebacitracins. The results over time withinthe periods under study suggest a decreas-ing effect of growth promotants on dailyweight gain and feed efficiency. A slightdecrease in efficacy over time has alsobeen reported by Rosen [351. However,one has to consider the use of more potentpreparations of therapeutical type in thebeginning of this period compared withless potent ones in more recent times, suchas the antibiotic promotants approved inthe EU and listed in table II. When com-

paring tylan responses on growth rate andfeed efficiency in growing-finishing pigs,Schneider [38] was unable to find differ-ences in responses in the period of 1969/79versus 1980/90 (table II[). However, thetrend of increasing the level of dietary pro-motants with time has to be considered

[27, 35]. Unfortunately, the report bySchneider [38] does not give any infor-mation on this issue. Moreover, the changeover time in cost of promotants mightinfluence their level of inclusion. Thus inthe 25-year period 1967-93 the improve-ment in feed efficiency for broiler chick-ens needed to defray cost of, e.g., virginia-mycin has decreased from 4.3 to only

0.43% [35]. One would arrive at similarresults in calculations on pigs.

In further commenting some entries intable III, the extensive body of experi-mentation by Schneider [37J should bementioned, in which results from 35 Ger-man experiments with tylan performed inthe period 1969 to 1990 with a total of3800 pigs have been compiled. Informa-tion on the level of tylan inclusion is, how-ever, not given. This author arrived at rel-ative responses to tylan administration foraverage daily weight gains and feed effi-ciency of 3.1 and 4.2%, respectively, com-pared with unsupplemented control diets.

By comparing some commercial dietswithout and with supplementation ofantibiotics and fed to growing-finishingpigs kept under good environmental con-ditions, Hellberg [20] observed promot-ing effects on growth rate and feed effi-ciency of 3.4 and 1.9%, respectively. Infurther studies, the promoting effects ofZn-bacitracin were found to be 0.7 and

1.3%, respectively [21 ]. A general opinionis that growth and feed efficiencyresponses of pigs and of broiler chickensto antibiotic promotants is lower under

improved environmental conditions com-pared with poorer environments. Rosen[35] estimates the ratio in responsebetween a very good and a poor environ-ment to 1:2.

The main result of the data compiledin table III gives an average response bysupplementation of piglet diets with antibi-otic promotants in comparison with unsup-plemented control diets for growth rateand feed efficiency of 17 and 9%, respec-tively, which is the same value as givenby CEAS et al. [7]. In comparison withpiglets, corresponding responses for grow-ing-finishing pigs were inferior and aver-aged 3.6 and 3.1 % for growth rate andfeed efficiency, respectively. These val-ues are in good agreement with CEAS etal. [7], arriving at average values of 3.5and 3.0%.

There are difficulties in predictingresponses on performance in Swedish pigindustry to a re-introduction of antibioticgrowth promotants. As a result of changesin the country’s animal welfare rules, thecurrent rearing and production models andperformance levels differ from those inthe international experiments reviewed.Therefore, a lower response level on per-formance may be expected. In the pigletsector for growth performance and feedefficiency a response to antibiotic pro-motants of 4-5% may be assumed. For

growing-finishing pigs compared withpiglets a lower level of responses to pro-motant additives of 1.5-2% may also beassumed.

5. GROWTH AND FEEDEFFICIENCY RESPONSESTO PROMOTANTSIN POULTRY

As earlier outlined for pigs, there hasbeen a strong development in the use ofgrowth promotants in broiler chickens aswell as in layers since the 1950s [5].According to Garland [18!, the financialadvantage of feed costs by using antibi-otic promotants in the UK broiler chickenindustry may be calculated to be in theregion of 0.035 ECU per bird. On the basisof an annual production of 660 millionbirds, one arrives at an extra yield of23 100 tons of bird liveweight, and a sav-ing of about 91000 tons feed, which equalsa gross financial saving of 25 million ECUin the UK.

The main body of the experimentalwork on responses of broiler chickens with

respect to administration of promotantsdemonstrates an effect in comparison withthe unsupplemented control of between99 and 106% [5]. In poultry as well as inpig production, the technique of shuttlingevery 6th month between different growth-promoting preparations was introduced at

an early stage in order to avoid adaptationof the microbial flora to a single pro-motant.

Swedish and Danish experiments, per-formed during the period of 1967-76 withbroiler chickens fed Zn-bacitracin havebeen reviewed by Elwinger [ 12]. With theexception of one entry (in which the birdswere kept in cages), the broiler chickenswere raised in floor pens. The age at ter-mination of the experiments varied between36 and 56 days. The birds were fed dietssupplemented with between 5 and 20 ppmZn-bacitracin (in I entries). This supple-ment improved growth rate, on an average,by 2.0°!o and feed efficiency by 1.3% overthe unsupplemented control diets. Therewere no differences in mortality.

In correspondence with the result forpigs, responses in broiler chickens to pro-motants gave growth rates and feed effi-ciencies that were superior in the firstphase of development compared with thesecond. This is also in agreement with thesituation in turkeys as reported by Kuther125]; table IV).

In a comprehensive review, Rosen [36] [investigated the nutritional effects of tetra-cyclines (546 entries) and Zn-bacitracin(483 entries) in broiler chicken diets byusing multi-factorial regression analysis.The model included dietary concentrationof growth promotant, weight gain, feed effi-ciency, duration fed, gender, presence ofdisease and anticoccidial use. The resultswere also economically evaluated. Mini-mum levels of growth promotants havebeen calculated. Heavyweight birdsresponded better than lightweights. Zn-bac-itracin was superior to tetracyclines, mainlyas a result of better feed conversion ratiosand more limited variation in effects. Atthe supplementation level of Zn-bacitracinpresently recommended, and by using themodels worked out by this author [36], onearrives at responses in growth rate and feedefficiency of 2 and 3%, respectively. It wasalso observed that the promotants were

more effective with respect to live weightgains when used in diseased than in appar-ently healthy birds. By including anticoc-cidials the growth-promoting effect of thepromotants themselves was clearly limited,depending on the fact that anticoccidialshave a growth-promoting effect as well.As a general comment on this investiga-tion, one should recognize that today’s rec-

ommended dosage for promotants hasincreased compared with when they wereintroduced. This increase in recommended

dosage over time could be a result ofdecreasing cost per active unit and/or a wayto keep disease level low.

As reported by Bartov [ 1 ] (see tableM, avilamycin supplementation improved

the energy value (AME) over the unsup-plemented control diet by 2.5%. Recently,Schutte et al. [40] reported an improve-ment in the digestibility of gross energy,N, P and amino acids for adult roosters asa result of supplementing a diet with20 ppm virginiamycin.

As a beneficial effect in addition to

growth promotion, the inclusion of pro-motants has often been reported toimprove litter quality, which is a result ofdecreasing excreta moisture content [13,14]. This may be regarded as an advan-tage for bird hygiene and health, but alsoimproves labour and bird environment bydecreasing NH3 formation and environ-mental air pollution as well [ 15].

The overall responses of broiler chick-ens to the promotants listed in table IV as

regards growth rate and feed efficiency incomparison with unsupplemented controldiets may be calculated to be, on average,3.9 and 2.9%, respectively. These meanvalues are in fairly good agreement withthose given by CEAS et al. [7] of 4% forboth traits. However, the value of 2% forgrowth rate based on Rosen [36] is muchlower. This contrast could possibly beexplained by zero and negative responsesto promotants being noticed in a signifi-cant part of the experiments compiled byRosen [35].

A re-introduction of antibiotic growthpromotants into today’s Swedish broilerchicken industry would certainly implyresponses in performance and feed effi-ciency at a lower level than mentionedearlier. Explanations of this are that theSwedish broiler industry has introducedproduction models without the use ofantibiotic promotants, with a very highstandard of animal hygiene and by the useof feeding programmes including admix-ture of anticoccidials and enzyme prepa-rations. A tentative response level for per-formance and feed efficiency of 1-1.5%may be assumed.

6. ENVIRONMENTALIMPLICATIONS OF FEEDINGANTIBIOTIC PROMOTANTS

As reviewed previously, the feeding ofantibiotic promotants improves pig andpoultry growth rate and feed efficiency.The response in younger animals is supe-rior to that of more adolescent individu-als. The superior growth rate of animalsmeans that the turn-over rate of a certainbatch of animals is speeded up, leading toan economic advantage for promotantfeeding. From an economic point of view,the improved feed efficiency is, however,of predominant importance.

As a consequence of the improved feedefficiency, the amounts of nutrientsexcreted by the animals as faeces and urineare lowered in proportion to the decreasedamount of feed consumed by the animals,i.e., by approximately 3-4%. For pig andpoultry production based on cereal diets,this level corresponds to a relative decreasein nutrient discharge of 15-20%. Accord-ing to the present literature review on poul-try and pigs, dietary administration ofantibiotic promotants does not noticeablyaffect nutrient absorption. However, aminoacid balances have been demonstrated tobe improved in animals fed antibiotic pro-motants. On the other hand, any protein-saving effects beyond the lowered amountof feed needed per bird have yet to beproven.

In poultry, antibiotic dietary inclusionhas been shown to improve litter quality.Litter quality has also been shown to affectNH3-formation [ 15]. As a consequence,housing environment may be expected tobe improved by antibiotic promotant feed-ing, which also leads to an impact for theexternal environment. With respect to thefact that ionophoric additives have effectssimilar to those of antibiotic promotants,one could speculate that the environmen-tal effects mentioned are brought aboutby ionophores as well.

7. ECONOMIC IMPACT OFPROMOTANT WITHDRAWALIN THE EU

According to De Craene and Viaene[9] studying the economic effects ofgrowth promotants for livestock produc-tion within the EU by model calculationsat farm level, a withdrawal of antibioticgrowth promotants would imply a rise inproduction costs of up to 8.2% for pigmeat. On withdrawal, the pig meat pricewould rise and intra-Community tradewould be affected. For the entire EU,exports would decrease, which wouldreduce expenditures on export refunds. Inthe pig meat sector, the annual reduction ineconomic benefits would amount to1.21*10! ECU, of which the consumerswould have to bear 48% and the producers52%. The consumers would buy smallerquantities of higher priced meat productsand would try to find substitutes. For poul-try meat and eggs at farm level, productioncosts would increase by 3.4 and 1.2%,respectively. The demand for eggs woulddecrease only slightly, but total loss ofbenefits in the EU would annually be29* I 06 ECU, of which the consumerswould bear 70% and the producers 30%.On withdrawal of promotants, broiler meat

production is expected to increase by3.4%. In this sector, the annual economicbenefits would decrease by 229 106 ECU,of which 57% have to be borne by the pro-ducers and 43% by the consumers.

Production costs for beef wouldincrease by 6% and would be followed bya slight decrease in demand. Economicbenefits would be lowered by 820* 106ECU. In the dairy cattle sector, withdrawalof promotants is expected to increase pro-duction costs by 4.6%. However, thisincrease would not affect demand. Thiswould result in a forcing out of the lessefficient farmers, their milk quotas beingbought by more efficient farmers.

It might be stressed that these calcula-tions are based on today’s situation in theEU. Future changes in subsidy levelstransferred to different sectors of EU agri-culture will certainly have an impact onthe outcome of this type of calculations.

8. CONCLUSION

Pig and poultry responses to dietaryinclusion of antibiotic promotants in termsof growth performance and feed efficiencyas compared with unsupplemented con-trol diets are higher in the first phase thanin the second phase of the growing period.Thus, piglets respond more clearly thangrowing pigs (20-50 kg), and these againrespond more efficiently than finishingpigs (50 kg to slaughter). In the latter classof animals promotant effects seem to beminute. In poultry, promotant effectsdecline correspondingly. Responses topromotants of a specific type in recenttime seem to be of the same magnitude ascompared with 20 years ago, although forsome preparations the recommended doseshave increased. Obviously, antibiotic pro-motants decrease animal morbidity. Thegrowth performance response of growing-finishing pigs and broiler chickens to pro-motant additives presently approved in theEU is 3 to 4% compared with unsupple-mented control diets. For feed efficiency inpigs, as well as in poultry meat produc-tion, the values are slightly lower. The rel-ative responses to antibiotic promotantsare lower under good environmental con-ditions than under poor. From an eco-nomic point of view, responses in feedefficiency are of greater importance thangrowth performance. Promotant dietaryinclusion also leads to improvements(labour and external) through lower exc-reta nutrient discharges in pigs and poul-try, and probably also lower NH3 forma-tion in poultry litter.

ACKNOWLEDGMENTS

This review was published in the journalof the Royal Swedish Academy of Agricultureand Forestry 136 (19) (1997) 9-21. Permis-sion to reprint it was kindly granted by theRoyal Swedish Academy of Agriculture andForestry.

REFERENCES

[ 1 ! Bartov I., Effect of growth promoters on mon-ensin toxicity in broiler chicks, Br. PoultrySci. 35 (1994) 123-133.

[21 Bates J., Jordens J.Z., Griffiths D.T., Farmanimals as putative reservoir for vancomycin-resistant enterococcal infection in man, J.Antimicrob. Chemother. 34 (1994) 507-514.

[3] Beck H., Gropp J., Payzone bei SPF-Schweinen, Landwirtschaftl. Forsch. 28(1973) 25-30.

[4 ! Begley S., The end of antibiotics, NewsweekThe International, March 28 (1994) 39!1.

[51 Brenninkmeiyer C., The use of antimicro-bials as growth promoters in poultry, Proc.XX World’s Poultry Congress, New Delhi,India, 1996, Vol. 11, 119-124.

[61 Broz J., Oldale P., Perrinvoltz A., Effects ofTrichoderma viride enzyme complex on per-formance of broiler chickens receiving pel-leted diets, Arch. Gefliigelkd. 58 (1994)182-185.

[7 ! CEAS Consultants et al., The impact of ani-mal husbandry in the European Communityof the use of growth promoters in animal feed,Vol. 1, 2, E.C., Brussels, February 1991,319 p.

[81 Cromwell G.L., Davis G.W., MorrowW.E.M., Prime R.A., Rozeboom D.W., SimsM.D., Stanisiewski E.P., Ho C.H., Efficiencyof the antimicrobial compound U-82,127 as agrowth promoter for growing-finishing pigs,J. Anim. Sci. 74 (1996) 1284-1287.

[9] De Craene A., Viaene J., Economic effectsof technology in agriculture. Do performanceenhancers for animals benefit consumers’?,Report, University of Ghent, Fac. Agric. Sci-ences, Dept. of Agro-Marketing, 1992, 162 p.

[101 Decuypere J.A., Dierick D.A., VervaekenLJ., Henderickx H.K., Intluence of virginia-mycin on the digestive physiology in pre-caecal re-entrant cannulated pigs. Arch. Anim.Nutr. (Berlin) 41 (1991) 373-393.

[ 1 ] ] DuPont H.L., Steele J.H., Use of antimicrobialagents in animals’ feeds: Implications inhuman health, Rev. Infect. Dis. 9 (1987)447-460.

[ 121 Elwinger K., Sammanstiillning over danskaoch svenska forsok med tillv5xtstimulerande

5mnen (fr5mst zinkbacitracin och payzone)i foder till fjdderf5, Report, Dept. AnimalNutrition and Management, Swed. Univ.Agric. Sciences, Uppsala, Sweden, 1976,1 p. (in Swedish).

[ 13 ! ] Elwinger K., Engstr6m B., Bemdtson E., Fos-sum O., Tcg]6f B., Effect of avotan

(avoparcin) and maxus (avilamycin) on thecaecal growth of C. per/ringens and the occur-rence of necrotic enteritis in broilers, ReportDept. Animal Nutrition and Management,Swed. Univ. Agric. Sciences, Uppsala, Swe-den, 1993.

[ 14! ] Elwinger K., Engstr6m B., Bemdtson E., Fos-sum 0., Waldenstedt L., Effect of growthpromoters and coccidiostats on performanceand growth of C. perfringens in the caeca ofbroilers, Proc. XX World’s Poultry Congress,New Delhi, India, 1996, Vol. II, 219.

[ I S ! ] Elwinger K., Svensson L., Effects of dietaryprotein content, litter and drinker type onammonia emission from broiler houses,J. Agric. Enging. Res. 64 (1996) 197-208.

[ 16! ] Fiems L.O., Cottyn B.G., Demeyer D.I., Ani-mal biotechnology and the quality of meatproduction, Papers presented at OECD Work-shop, Melle, Belgium, in: Developments Ani-mal and Veterinary Sciences 25, Elsevier,Amsterdatn, 1991. 1 .

[17! ] Fr6lich A., Kvarnfors E., Månsson I., Simon-sson A., Antibiotic additives in sows’ diet.Effects on production and intestinal flora,Acta Agric. Scand. 24 ( 1974) 273-285.

[ l 8 ! ] Garland P.W., Range of substances currentlyavailable and problems to be addressed forthe future, Proc. World’s Poultry Sci. Asso-ciation, lOth Eur. Symp. on Poultry Nutr.,Antalya, Turkey, 1995, 203-207.

[19! ] Gruber F., Einfluss der Di-N-Oxide auf dieFutteraufnahme beim Schwein. Dissertation,Ludwig-Maximilians-Univ., Munchen, Ger-many, 1986.

[201 Hellberg A., Redogbrelse for utf6rd provn-ing av saluf6rda svinfoderblandningar, Svin-skbtsel 9 (1965) 233-239 (in Swedish).

[21 ! 1 ] Hellberg A., Redogbrelse för jämförandef6rs6k med olika antibiotika i fodret till slak-

tsvin, Öllsjö 1967, Svinsk6tsel 3 (1968)75-78 (in Swedish).

[22! ] Hofshagen M., Kaldhusdal M., Barley inclu-sion and avoparcin supplementation in broilerdiets. I. Effects on small intestinal bacterialflora and on performance, Poultry Sci. 71 1(1993)959-969.

[231 Hudd D.L., The addition of antibiotics infeedingstuffs, in: Bogan J., Lees P., JoxallA.T. (Eds.), Pharmacological Basis of LargeAnimal Medicine, Blackwell Sci. Publica-tions, Oxford, 1983, 107-128.

[241 Korniewicz A., Klawe A., Kirschke A.Paleczek B., Effect of tylosin, bayonox andridzol on growth and feed utilization ofpiglets, Roczniki Naukowe Zootechn. 23(1985)269-279.

[25] Kuther K., Experience with virginiamycin inGerman broiler production. Proc. EskalinBroiler Symp, 8 March, London, 1979,32-35.

[26] Laming G.E., Growth promoters, in: FutureProduction and Productivity in LivestockFarming. Developments in Animal and Vet-erinary Sciences, Elsevier, Amsterdam, 20(1986) 127-148.

[271 [ Lange S., Ek E., On putting the argument forbanning or tightly controlling the use ofantibiotics as feed additives, Proc. World’sPoultry Sci. Assoc., lOth Eur. Symp. Poul-try Nutrition, Antalya, Turkey, 1995, 1 I p.

[28 J Langhout D.J., Schutte J.B., Effects of antibi-otics and xylanase enzyme preparation aloneor in combination on broiler performance,ILOB report Nr. I94-3895, Wageningen, theNetherlands, 1994, 21 p.

1291 Lindermeyer H., R6hrmoser G., Gradl B.,Markenfleischerzeu-gung mit oder ohne Leis-tungsf6rderer, Schule und Beratung, 9-10( 1993) 4 p.

[301 McCutcheon S.N., The use of growth pro-moting agents, in: Purchas R.W., Butler-HoggB.W., Davies A.S. (Eds.), Meat productionand Processing, New Zealand Soc. AnimalProd. Occ. Public., 1989, 11, 113-123.

[31 1] Myers D.J., Speer V.C., Effects of antibioticand flushing on the performance of sows withshort farrowing intervals, J. Anim. Sci. 36(1973) 1125-1128.

[32 ! Noussiainen J., Suomi K., Comparative obser-vations on selected probiotics and olaquin-dox used as feed additives for piglets aroundweaning. I . Effect on the bacterial metabolites

along the intestinal tract, blood values andgrowth, J. Anim. Physiol. Anim. Nutr. 66(1991)212-223.

[331 Richter A., L6scher W., Witte W., Leist-ungsforderer mit anti-bakterieller Wirkung:Probleme aus phannakologisch- toxikolo-gischer und mikrobieller Sicht, Prakt. Tier-arzt 77 ( I 996) 603-624.

[341 Robertsson J.A., Lundeheim N., Prohibiteduse in antibiotics as a feed additive for growthpromotion - effects on piglet health and pro-duction parameters. Proc. l3th Intern. PigVet. Soc. Congr., 282. Bangkok, Thailand,1994.

[35 [ Rosen G.D., Antibacterials in poultry and pignutrition. In: Wallace R.J., Chesson A (Eds.),Biotechnoloy in Animal Feeds and Feeding,VCH Verlagsgesellschaft mbH, Weinheim,Germany, 1995, pp. 143-172.

[361 Rosen G.D., The nutritional effects of tetra-cyclines in broiler feeds, Proc. XX World’sPoultry Congress, New Delhi, India, 1996,Vol. II, 141-146.

[371 Schneider W., Wirkung des Fut-terzusatzstoffes Tylan G in der Schweine-mast. I. Mitt. Analyse deutscher Versuchs-ergebnisse, Schweinezucht und Schweinemast40 (1992) 3.

[38] Schneider W., Wirkung des Futterzusatzt-soffes Tylan G in der Schweinemast. 2. Mitt.Leistungsf6rdernde Effekte, Schweinezuchtund Schweinemast 40 ( 1992) 1 18-121. 1.

[391 [ Schurz M., Jeroch H., The influence of antibi-otic and enzyme addition to a barley-basedration on fattening performance and somecharacters of carcass composition and meatquality of broilers, Proc. 9th Eur. PoultryConf., Darvel, the UK branch of the WPSA,1994, pp. 441-442.

[401 Schutte J.B., Beelen G.M., Boselli E., Effectof virginiamycin on apparent ileal digestibil-ity of dietary nutrients in adult roosters, Proc.9th Eur. Poultry Conf., 7-12 August 1994,Glasgow, 1994, Vol. I, 443-444.

[41 ! Schutte J.B., de Jong J., Boselli E., Interactioneffects of virginiamycin and a xylanaseenzyme preparation on broiler performance,Proc. 9th Eur. Poultry Conf., 7-12 August1994, Glasgow, 1994, Vol. 1, 445-446.

[421 Soma J.A., Speer V.C., Effects of PMS andchlortetracycline on the reproductive effi-ciency of sows, J. Anim. Sci. 41 (1975)10(l-105.

1431 SOU, Antimicrobial feed additives, Reportfrom the Commission on Antimicrobial FeedAdditves, Fritzes fbrlag, Stockholm, 1997,356 p.

[44] Speer V.C., Reducing farrowing intervals insows, Feedstuffs U.S.A. 46 (1974) 20-3 1.

[45] Tarrago J., Sanz R., Puchal E., Tylosin andvirginiamycin as growth promotants in youngpigs, Anim. Prod. 26 ( 1978) 359.

[461 Tid6n A., Fbrs6k med flavomycin i slakt-svinsfoder. Grupper med och utan f6rbehan-dlingsfoder samt jämförelse mellan olikaergotroper, Report Dept. Animal Nutritionand Management, Swed. Univ. Agric. Sci-ences, Uppsala, Sweden, 1974, 14 p. (inSwedish).

[471 Verbeke W., Viaene J., Experimental impactof using feed additives. Economic implica-tions and legal environment in the Benelux,Report, Univ. Gent, Fac. Agric. and AppliedBiol. Sciences, Dept. Agric. Economics, 1996,43 p.

[481 [ Zivkovic S., Zlatic H.. A review of ten yearsof experience in feed additives in pig dietson large-scale farms in Yugoslavia. LivestockProd. Sci. 6 (1979) 61-66.