In Practice (2005) 27, 37-43

Problems of antibiotic resistance in pigs in the United Kingdom

David Burch

Introduction
The fact that large quantities of antimicrobials are used in pig production in the United Kingdom has led to the assumption that antimicrobial resistance must be posing major problems. This, in turn, raises a number of pertinent questions. For example, do veterinary practitioners feel that resistance is compromising the successful treatment of their patients? Are antimicrobials over used in pigs or are they not used prudently? Finally, does antimicrobial use in pigs have an adverse effect on humans, either directly from the transmission of resistant zoonotic pathogens or indirectly through the transmission of antimicrobial resistance via commensal organisms? This article reviews recent data on antimicrobial usage and resistance problems in pigs, with a view to shedding light on these questions and related issues.

Antimicrobial usage in veterinary medicine and in pigs
The Veterinary Medicines Directorate recently published data on the use of antimicrobials in veterinary medicine in the UK, covering the period 1998 to 2002 (VMD 2003). The overall use of therapeutic products over the last five years has been relatively static ranging from 445-462 tonnes between 1998 and 2002 with 457 tonnes being used in 2002. This is in spite of a fall in pigs slaughtered of about 37% during this period. However during this time several antimicrobial growth promoters were withdrawn, some of which had disease-preventing effects. Furthermore, a major new immuno-suppressive infection postweaning multi-systemic wasting syndrome (PMWS), associated with porcine circovirus type 2, swept the country resulting in the increased use of therapeutic antimicrobials. The major product groups are highlighted in Graph 1.

Graph 1. Major therapeutic antimicrobial groups used in veterinary medicine

THERAPEUTIC ANTIMICROBIALS
As can be seen, tetracyclines account for the greatest quantities of active substance used (217 tonnes (47%) in 2002) and this is primarily due to the use of chlortetracycline feed premixes, which are commonly used for treating respiratory infections in both pigs and poultry. In pigs they are primarily given for Mycoplasma hyopneumoniae (enzootic pneumonia), Pasteurella multocida and Actinobacillus pleuropneumoniae infections. Trimethoprim/sulphonamide combinations are the second mostly commonly used products (at 88 tonnes (19%) in 2002). They are used for the treatment of both respiratory and enteric bacterial disease, especially Escherichia coli and Salmonella species infections in weaner and growing pigs, which have increased in PMWS-affected herds. These products are available in water-soluble, piglet doser and injectable forms as well as feed premixes. The use of beta-lactams, which include penicillins and synthetic penicillins such as ampicillin and amoxycillin, has been relatively stable at around 60 tonnes (13%). The penicillins are popular as feed premixes (eg penicillin V and amoxycillin) but also as soluble forms for poultry in particular. Macrolides, mainly in the form of tylosin premix, have seen a marked increase in use in recent years. Since the ban on the use of tylosin as a growth promoter was introduced in 1999, its therapeutic use under prescription for porcine proliferative enteropathy (‘ileitis’) and enzootic pneumonia has increased steadily to 56 tonnes (12%) in 2002. Aminoglycosides have fluctuated in volume, but in2002 account for 22 tonnes (5%). The main premixes are neomycin and apramycin, which also come in soluble and oral doser forms for piglets and are commonly used for E. coli and Salmonella species infections. Fluoroquinolones are not widely used in the UK in tonnage terms. There are no feed premix formulations but there are water-soluble preparations for poultry (in particular, turkeys) and calves, and also injectables and piglet dosers. 

The ‘others’ group includes the pleuromutilins, tiamulin and valnemulin and the lincosamides, which are primarily used for swine dysentery, colitis and ileitis, caused by Brachyspira hyodysenteriae, B. pilosicoli and Lawsonia intracellularis respectively, as well as M. hyopneumoniae infections. They have shown very little fluctuation in recent years, with 13 tonnes (3%) used in 2002.

Route of administration
In its report, the VMD also reviews the use of therapeutic antimicrobial products by route of administration, but unfortunately the data is not broken down according to individual species, although efforts are being made to apportion the results in the future. In 2002, the medicated feedingstuff route accounted for 307 tonnes (67%) the oral and water route 110 tonnes (24%), injectables 34 tonnes (7%), intramammary 4 tonnes (1%) and others mainly topicals 2 tonnes (<1%) (see Graph 2).

In-feed medication is the preferred route of preventing and treating infections in pigs, because it requires very little labour on the farmer’s part; injections, on the other hand, are very laborious. In general, the cost of in-feed products is relatively low in comparison with water solubles and injectables; for example, the cost of chlortetracycline in feed is 1.5p, and in water 27.5p/gram of active substance, whereas oxytetracycline injection costs 65p/gram. This may not be totally representative of all antimicrobial product ranges, but it demonstrates the value in cost/benefit terms of in-feed medication and explains why in-feed chlortetracycline is the principal product used.

Graph 2. Comparison of route of administration of antimicrobials

Use in pigs
Precise usage figures for different species are difficult to calculate, as many of the products are used in more than one, but estimates would suggest that 40-45% of therapeutic antimicrobials are used in pigs.

OTHER ANTIMICROBIALS
Growth promoters
Growth promoters accounted for an additional 27 tonnes of antimicrobial usage in 2002. The major ones in the UK of ‘resistance concern’, because they were related to antimicrobials used in man, are avoparcin (a glycopeptide – related to vancomycin in man), virginiamycin (a streptogramin – related to dalfopristin-quinupristin), zinc bacitracin (bacitracin) and tylosin (a macrolide – related to erythromycin). All of these are no longer in use, having been withdrawn in mid-1999 or before, under the ‘precautionary principle’. The remaining ones, which will be withdrawn 31st December 2005, are avilamycin, flavophospholipol, salinomycin in pigs and monensin in cattle; these growth promoters are not currently associated with resistance transfer issues, as neither they, nor any related compounds, are used in humans.

Coccidiostats
The amount of antimicrobials used for the control of coccidiosis in pigs is relatively small compared to that used in poultry (250 tonnes in 2002). Resistance to products such as toltrazuril in piglets does not appear to be a problem.

Effect of antimicrobial use on the development of resistance in pigs
A report on antimicrobial sensitivity of isolates in 2002 has been recently published by the Veterinary Laboratories Agency (VLA 2004). E. coli is a useful marker bacterium, across all species of animal, for showing (albeit not in absolute terms) where antimicrobial resistance lies. It is an organism that readily gains resistance to many antimicrobials, so is also a reasonable indicator of antimicrobial use.

The antimicrobial disc diffusion test is the main technique used for determining sensitivity. It involves growing organisms on Isosensitest agar plates (Oxoid) with media supplementation for fastidious organisms. The uniform cut-off point for resistance and sensitivity is a 13mm diameter zone of inhibition around the disc. This method has been standardised at all the VLA’s regional veterinary laboratories. Many of the organisms may have come from animals that have been treated with antimicrobials and will therefore have been under selective pressure. The tests are relatively simple, so may either over- or underestimate the sensitivity of an organism to a certain antimicrobial. The minimum inhibitory concentration (MIC) test, coupled with the pharmacokinetic data of the antimicrobial, is a more accurate way of assessing sensitivity; nevertheless for monitoring purposes though, disc diffusion remains a very useful method.

Table 1. Comparison of antimicrobial resistance (%) in E. coli from different animal species of all ages (2002)
Antimicrobial / disc strength	Pig	Cattle	Sheep	Avian	
No of isolates	365	4193	299	141	
Ampicillin 10µg	43	44	22	48	
Amoxycillin/clavulanate 20/10 iu	-	14	3	-	
Tetracycline 10µg	85	48	36	62	
Neomycin 10µg	11	26	14	12	
Apramycin 15µg	12	3	2	4	
Trimethoprim/sulphonamide 25µg	52	23	13	33	
Enrofloxacin 5µg	8	0.1	0	3	

From these figures it can be seen that there is a high level of resistance in porcine E. coli to tetracycline and trimethoprim/sulphonamide combinations. Avian isolates also show high resistance to these two antimicrobials. Of interest is the level of fluoroquinolone (enrofloxacin) resistance in pigs, which has been quite low in the past but has recently increased.

Table 2. Comparison of antimicrobial resistance (%) in E. coli from pigs of different age groups and from ones expressing the K88 (F4) antigens (2002)
	<1month	1-6 months	>6 months	All ages	K88	
No of isolates	114	195	15	365	52	
Ampicillin10µg	44	44	40	43	54	
Tetracycline 10µg	85	90	60	85	94	
Neomycin 10µg	11	10	7	11	8	
Apramycin 15µg	16	11	0	12	23	
Trimethoprim/sulpha 25µg	58	49	67	52	65	
Enrofloxacin 5µg	11	4	20	8	13	

E. coli infections usually affect young suckling pigs (neonatal scours) and, in particular, the weaned pig at around 28 days of age and are often associated with strains expressing the K88 antigen (now reclassified as the fimbrial antigen F4). Thereafter, they tend to subside with occasional cases of bowel oedema being seen in growing pigs. In adults, E. coli particularly affects the sow at the time of farrowing, causing the so-called mastitis-metritis-agalactia (MMA) syndrome and may be associated with vulval discharges and infertility later on. 

Levels of resistance tend to be higher in younger suckling pigs, where more sophisticated antimicrobials are applied individually, especially by piglet doser or by injection. The category of pigs over six months of age (presumably periparturient sows) shows a surprisingly high level of resistance, but there are relatively few isolates (15) and in the report notes that two of the three enrofloxacin isolates came from the same farm causing this wide fluctuation (VLA, 2004).

Overall, the apparent trend over the period 1998 to 2002 has been for increased E. coli resistance to tetracyclines, trimethoprim/sulphonamides and the fluoroquinolones; little net change to the aminoglycosides (apramycin and neomycin); and decreased resistance to ampicillin during.

Graph 3. E. coli resistance (%) to various antimicrobials in pigs

This has been an interesting period for pig production, as 1998 not only saw the start of the collapse of production in the UK, but also the emergence of PMWS, subsequently spread across the UK. Initially, this disease, which is associated with the destruction of the lymphoid immune system, caused up to 30% mortality, but gradually mortality fell to about 5%, and it still tends to grumble on at around this level. PMWS-affected herds experience an increase in diarrhoea (53% of cases) due to mixed infections, respiratory disease (68% of cases) and systemic infections caused especially by Streptococcus suis and Haemophilus parasuis in particular. As mentioned earlier, the need to control these secondary bacterial infections would account would account for the higher usage in feed of chlortetracycline and trimethoprim/sulphonamides in spite of the fall in pig numbers. It is surprising that the aminoglycoside has remained relatively static; however there is still a substantial use of zinc oxide in weaner feeds to prevent E. coli diarrhoeas and this has a major benefit of reducing the use of, and resistance development pressure on, the aminoglycosides.

The development of resistance to fluoroquinolones in animals is a great concern in relation to the possible transmission of resistant organisms to humans, where these medicines are considered essential for the treatment of potentially terminal cases. Pressure is being applied to bring about the withdrawal of these products for oral use of in food animal medicine, particularly in the USA where a court case is ongoing to stop their use in poultry. Fluoroquinolones are not permitted for use in pigs in the USA and they are not used in food animals in Australia.

Graph 4. Fluoroquinolone (enrofloxacin) resistance development trend in E.coli from pigs

From Graph 4, enrofloxacin resistance in E. coli isolates from pigs of all ages doubled between 2000 and 2002, which is a potential concern. However, the majority of isolates were from piglets less than one month old, whereas resistance was relatively low in finishing pigs of slaughter age (0ne to six months). The majority of isolates have the K88 antigen.

In its report, VLA also covered a number of other important pathogens in the pig, including Arcanobacterium pyogenes which causes abscesses, often following tail biting.

Table 3. Comparative resistance (%) of other porcine bacteria to various antimicrobials (2002)
	Pasteurella multocida	Actinobacillus pleuropneumoniae	Strep suis	A. pyogenes	
No of isolates	161	54	16	20	
Ampicillin10µg	3	4	0	0	
Penicillin 10iu	-	-	0	0	
Tetracycline 10µg	9	22	94	0	
Trimethoprim/sulpha 25µg	8	13	6	10	
Enrofloxacin 5µg	0	4	0	0	
Ceftiofur 30µg	-	0	0	0	

There has been very little change in the development of antimicrobial resistance by these organisms in recent years. Over 90% of P. multocida isolates are still sensitive to the tetracyclines, in spite of the widespread use; A. pleuropneumoniae is less sensitive, albeit 78% is still a high proportion. Unfortunately there are no vaccines for A. pleuropneumoniae commercially available in the UK. S. suis is largely resistant to the tetracyclines but remains completely sensitive to the penicillins, synthetic penicillins and cephalosporins, as does A. pyogenes. 

A. pleuropneumoniae can be a difficult organism to treat but, fortunately, remains generally susceptible to trimethoprim/sulphonamide and ampicillin. It shows little resistance to enrofloxacin, which is administered by injection. This may be due to an increase in the use of fluoroquinolones in PMWS cases, where, due to the destruction of the immune system, better efficacy is achieved with bactericidal antimicrobials that kill the organism directly rather than bacteriostatic ones that require the assistance of the immune system to clear up the infection. It is for similar reasons that aminoglycosides and fluoroquinolones have become so important in human medicine to treat patients who are immunocompromised following radiotherapy, chemotherapy for cancer or transplantation or are infected with human immunodeficiency virus (HIV).

So far, although there have been some high levels of tetracycline and trimethoprim/sulpha resistance reported in E. coli in pigs, the same does not appear to be true for the bacteria associated with respiratory disease, such as P. multocida and A. pleuropneumoniae and (although not included in the VLA report) H. parasuis and M. hyopneumoniae. S. suis, the cause of meningitis and arthritis, is still highly sensitive to the penicillins. Thus, it can be seen that the development of resistance is both antimicrobial and organism specific. 

With regard to enteric bacteria other than E.coli, there are a number of infections seen in the grower pig, such as swine dysentery, colitis and ileitis caused by B. hyodysenteriae, B. pilosicoli and L. intracellularis. The former two are difficult to culture and sensitivity testing is not routinely carried out, but MICs can be determined. The third is only cultured in cell cultures and antimicrobial sensitivities are likewise difficult to carry out; however, an intracellular MIC has been established for a few isolates.

Table 4. MIC 50, MIC 90, range and estimated breakpoint (µg/ml) for various antimicrobials against B. hyodysenteriae and B. pilosicoli
B. hyodysenteriae*	Valnemulin	Tiamulin	Lincomycin	Tylosin	
MIC 50	0.031	0.125	16	>256	
MIC 90	0.5	1.0	64	>256	
Range	<0.016-2.0	<0.016-2.0	<1-64	<2->256	
B. pilosicoli**					
MIC 50	0.06	0.125	32	>512	
MIC 90	0.5	1.0	64	>512	
Range	0.03-2.0	0.06-8.0	>512	<16->512	
Estimated breakpoints	>4	>4	>35	>50	
L. intracellularis***					
Intracellular MIC	<2	4	32	64	
*Karlsson et al 2002 (75 Australian isolates); ** Kinyon et al, 2002 (25 N. American isolates); *** McOrist et al, 1995 (2-3 UK isolates)

MICs provide very useful information as they give the activity of the antimicrobial for a particular isolate or, in the case of the MIC 50 or MIC 90, for 50% or 90% of the isolates respectively (see Table 4). This can be related to the maximum concentration of the antimicrobial found in the gut and an effective level, or ‘breakpoint’ can be estimated. So, although the MICs for valnemulin against the Brachyspira species look low, the concentration achieved in the colon is also quite low; conversely, for lincomycin the concentration is quite high but the MICs are high and at the top of the range there is definite resistance. For tylosin, there is resistance even at the MIC 50, suggesting it is of limited value for these conditions. Whether this is because the product was used as a growth promoter is debatable. Organisms tend to develop resistance to tylosin quite quickly, whereas resistance to the pleuromutilins and lincomycin develops in a much slower ‘stepwise’ fashion. Karlsson et al (2002) demonstrated an interesting pattern of susceptibility by B. hyodysenteriae (see Graph 5). 

Graph 5. Pattern of B. hyodysenteriae susceptibility to various antimicrobials

All of these products, except valnemulin, have been available for over 20 years, so the pattern of resistance has become established by the mode of action of the antibiotic rather than just its use. The wave-like patterns may indicate where mutations have occurred and frank resistance has developed (e.g. tylosin). There was some concern that there was resistance developing to tiamulin in the UK in the late 1990s but this has in general subsided with the introduction of valnemulin and the culling of less efficient infected herds. However, in Germany there is resistance to the pleuromutilins, which may have been exacerbated by the EU ban of the quinoxaline derivatives, carbadox and olaquindox for the prevention of swine dysentery and also the nitroimidazoles, dimetridazole and ronidazole, on safety grounds. Widespread resistance to the pleuromutilins would pose a major problem in the UK, as currently there are no other suitable alternatives. Culling of infected herds would have to be considered.

Current impact on clinical practice
From the pig practitioner’s point of view, antimicrobial resistance is not currently perceived as being a major clinical problem in the UK. There are usually suitable, effective, alternative antimicrobials available and, fortunately, a number of new molecules (albeit often related to, or derivatives of, older compounds) continue to be introduced such as florfenicol (chloramphenicol), tulathromycin and acetylisovaleryl tylosin (macrolides); a number are still under development.

Antimicrobials do appear to be widely used in the national pig herd, especially in comparison with, say, Denmark, where there has been a higher focus on herd health and disease eradication than in the UK. For example, in 2002, approximately 17 tonnes of active substance /million pigs slaughtered were used in the UK, compared with 3 tonnes/million pigs slaughtered in Denmark (Danmap, 2003). The UK industry finds itself in a poor competitive situation and has been in severe decline in recent years. Contributing factors have been the introduction of the ban on sow stalls and tethers, banning of the use of meat and bone meal in feed, the strength of sterling against the Euro, and PMWS (which did not appear in Denmark until 2002). With a declining industry, underinvestment and shortcuts are bound to occur, especially in the areas of hygiene and pen cleaning, which can lead to increased enteric disease and, as a result, greater reliance on antimicrobials.    

Transmission of resistance to man

ZOONOTIC PATHOGENS
The major potential zoonotic pathogens of concern are Salmonella and Campylobacter species and S. suis. The latter is transmitted relatively infrequently (approximately two cases/year), but has been found mainly in pig farm workers, slaughter men and butchers (i.e. those in close contact with pigs and meat; Barlow et al, 2003). Antimicrobial resistance is not a practical problem, as S. suis is still highly susceptible to the penicillins; however, immuno-compromised people are advised not to work with pigs as there is an increased risk of infection.

Of the campylobacters, Campylobacter coli is the dominant strain in pigs (>90% of isolates) whereas C. jejuni is the major cause of food poisoning in humans (>90% of cases) globally. A study using erythromycin resistance as a marker (Burch, 2002) and another involving genetic profiling of C. coli (Guevremont et al, 2004) have demonstrated that pig meat presents either a very low or no risk of transmission of campylobacter to humans. These are relatively fragile organisms and chilling of the carcase also helps to destroy them (Guertler et al, 2004). However, in some countries, such as Germany and Denmark, raw minced pig meat (like steak tartar) is consumed and this may increase the risk of transmission, although this is unproven as yet. Thus, if the risk of transmission is very small or even zero, so is the risk of transfer of antimicrobial resistance.

With regard to the transmission  of salmonellae from pigs to man, there is a definite reported link to Salmonella enterica serovar Typhimurium, as certain definitive types found in human S. Typhimurium cases are associated with specific porcine isolates DT 193 (13.6% pig isolates and 6.9% human isolates) and U310 (4.8% pigs and 3.2% human) (VLA, 2003). However, S. Typhimurium only accounts for 13.1% of total salmonella cases in man, where S. Enteritidis still predominates at 64.5% of cases and is mainly associated with chickens and eggs. According to the VLA report, S. Derby, which is found in 7.7% of incidents in pigs in 2002, was not recorded specifically in humans that year and is presumably well below the 1% level. S. Typhimurium is the dominant species isolated in pigs and can be invasive and found in meat tissues; sausages are reported to have a contamination rate of about 8%.

Table 5. Comparison of antimicrobial resistance (%) of all salmonella isolates by animal species
Antimicrobial	Pigs	Cattle	Sheep	Poultry	
No of isolates	309	862	192	1580	
Ampicillin 10µg	61	11	5	10	
Tetracycline 10µg	84	13	6	16	
Neomycin 10µg	7	0	0	7	
Apramycin 15µg	5	0	0	0	
Trimethoprim/sulpha 25µg	63	4	2	24	
Nalidixic acid 30µg	6	1	1	2	
Ciprofloxacin MIC >2µg/ml	0	0	0	0	
Ceftazidime 30µg	0	0	0	0	
Amikacin 30µg	0	0	0	0	
(Source: VLA, 2003)

Pigs do carry a relatively high resistance rate in comparison with other species (see Table 5), because of the dominance of S. Typhimurium (71% of isolates) in pigs. The resistance patterns are similar to those displayed by E. coli, with high resistance being seen to tetracycline, trimethoprim/sulphonamide and ampicillin. However, there is no resistance reported to ceftazidime (cephalosporin) and amikacin (aminoglycoside), which are two very important antimicrobials in human medicine. There is a 6% incidence of nalidixic acid resistance, which is an indicator of the first step in resistance development to the fluoroquinolones. However there is no reported ciprofloxacin (fluoroquinolone) resistance above the 2µg/ml MIC breakpoint commonly used; furthermore, only four out of 2943 reported food animal isolates above the 1µg/ml level and 5/2943 at the more sensitive 0.5µg/ml (0.3% in total) (VLA, 2004). Consequently, although salmonella may be transmitted to humans, the level of transfer of resistance to antimicrobials that are critical in human medicine is minimal.

COMMENSAL BACTERIA
Pigs are not usually associated with E. coli O157: H7 verocytotoxic strains, which are directly pathogenic in humans, and predominate in cattle. However, there is a potential risk of resistance transfer by ingestion of organisms, particularly by pig farm and slaughterhouse workers, and subsequently, to a lesser extent, by meat handlers along the food chain (where it becomes a food processing, preparation and hygiene issue). 

With regard to the enterococci, Enterococci faecium and E. faecalis, direct links have been demonstrated to pig farm workers, slaughterhouse workers and the community in general in Europe of vancomycin-resistant enterococci (VRE). However, a recent assessment of risk concerning a treatment failure in man associated with macrolide resistant E. faecium from pigs estimated the risk to be very small, with a probability of  less than 1 in 21billion (Doores et al, 2003). 

In Denmark, they have shown a marked fall in resistance in E. faecium from pigs since the removal of antimicrobial growth promoters tylosin, virginiamycin and avoparcin (see Graph 6).

Graph 6. Fall in resistance to various antimicrobial growth promoters following their removal by porcine E. faecium (Danmap, 2003)

Unfortunately there is no comparative data in the UK. However a similar picture is anticipated as the levels of E. faecium identified in a 1999/2000 slaughterhouse survey (Teale, 2002) showed tylosin resistance at a level of 90% and to quinupristin/dalfopristin 47%; however, vancomycin-resistant E. faecium was low, at 1%. The main concern has been with regard to immuno-compromised patients coming into contact with meat contaminated with vancomycin-resistant E. faecium, but it looks as if this potential route is almost eliminated. Nevertheless, there remains the important route of hospital-acquired VRE infections in immuno-compromised patients which are often epidemic and have been shown to be genetically from porcine isolates (Homan et al, 2002).

What is the state of play?
There is resistance in bacteria in pigs, but generally it does not appear to cause major clinical problems to the veterinary surgeon, as effective alternatives are currently available. There is no room for complacency, however, and these products should be used prudently. Vaccination and close attention to hygiene, management, feeding and biosecurity are necessary to maintain or, better still, improve the situation by helping to reduce dependency on antimicrobials.

On the question of resistance transfer to humans, the closer humans are to the pig in the production chain, the greater the risk of contamination. Clearly, pig farm and slaughterhouse workers are the most exposed. Further down the production chain, pig meat represents a potential risk; certainly, for S. Typhimurium, there is a risk of infection but apparently a low risk of transmission of resistance to the major antimicrobials used to control the infection in man. The new Zoonoses Action Plan, which was launched on behalf of the pig industry by the British Pig Executive in December 2000, and which classifies farms according to the incidence of positives to a meat juice ELISA for salmonella implements a clean-up programme for the worst affected, will also help reduce the level of contamination of carcases. With regard to campylobacters, there is a comparatively lower risk of transfer via pig meat. Similarly there is a low risk with E. faecium and the situation regarding VREs in the community is likely to have improved further following the removal of growth promoters.

Overall, the antimicrobial resistance situation in porcine veterinary medicine is fairly static and under control, although it is important to remain vigilant, especially given the forthcoming withdrawal of the remaining growth promoters. The transmission of salmonellae to humans does pose an on-going problem, but the risk of spread of resistance to humans, which might impair salmonella treatment, is low. C. coli resistance to macrolides is high but the risk of transmission is low. The risks of transmission of VRE to humans are expected to fall following the removal of the glycopeptide growth promoter avoparcin, but it will be interesting to see whether this actually reduces the incidence of infection in hospitals.

References
Barlow, A.M., Hunt, B.W., Heath, P.J. and Smith, R.M.M. (2003) The prevalence and clinical diseases caused in pigs by different serotypes of Streptococcus suis (June 2000 to September 2002) and human infection (1981 to October 2002) in England and Wales. Pig Journal, 51, 164-176

Burch, D.G.S. (2002) Risk assessment – Campylobacter infection transmission from pigs to man using erythromycin resistance as a marker. Pig Journal, 50, 53-58

Danmap (2003) DANMAP 2002 - Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. Eds Emborg, D-H. and Heuer O.E., Danish Veterinary Institute, Copenhagen, Denmark

Doores, S., Hurd, H.S., Hayes, D., Mathew, A., Maurer, J., Silley, P., Singer, R.S. and Jones, B. (2003) Low-level risk assessment for tylosin use in poultry and swine on the treatment of human food-borne disease. Proceedings Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, USA, Abst C2-1502

Guertler, M., Kasimir, S., Alter, T. and Fehlhaber, K. (2004) Prevalences of Yersinia enterocolitica and campylobacter spp from piglets to pork. Proceedings of the 18th International Pig Veterinary Society Congress, Hamburg, Germany, 2, p 658

Guevremont, E., Higgins, R. and Quessy, S. (2004) Characterisation of campylobacter isolates recovered from clinically healthy pigs and from sporadic cases of campylobacteriosis in humans. Journal of Food Protection, 67, 2, 228-234

Homan, W.L., Tribe, D., Poznanski, S., Li, M. Hogg, G., Spalburg, E. van Embden, J.D.A. and Willems, R.J.L. (2002) Multilocus sequence typing scheme for Enterococcus faecium. Journal of Clinical Microbiology, 40, 6 1963-1971

Karlsson, M., Oxberry, S.L. and Hampson, D.J. (2002) Antimicrobial susceptibility testing of Australian isolates of Brachyspira hyodysenteriae using a new broth dilution method. Veterinary Microbiology, 84, 123-133

Kinyon, J.M., Murphy, D., Stryker, C., Turner, V., Holck, J.T. and Duhamel, G. (2002) Minimum inhibitory concentration for US swine isolates of Brachyspira pilosicoli to valnemulin and four other antimicrobials. Proceedings 17th International Pig Veterinary Society Congress, Ames, Iowa, USA, 2, p. 50

McOrist, S., Mackie, R.A. and Lawson, G.H.K. (1995) Antimicrobial susceptibility of Ileal symbiont intracellularis isolated from pigs with proliferative enteropathy. Journal of Clinical Microbiology, 33, 5, 1314-1317

Teale, C. (2002) Antimicrobial resistance in porcine bacteria. Pig Journal, 49, 52-69

Veterinary Laboratories Agency (2003) Salmonella in Livestock production in GB 2002. Report for the Department for Environment, Food and Rural Affairs

Veterinary Laboratories Agency (2004) VLA antimicrobial sensitivity report 2002.
Report for the Department for Environment, Food and Rural Affairs

Veterinary Medicines Directorate (2003) Sales of antimicrobial products authorised for use as veterinary medicines, antiprotozoals, antifungals, growth promoters and coccidiostats, in the UK in 2002. Report for the Department for Environment, Food and Rural Affairs

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