Doi:10.1016/j.vetmic.2008.06.005

Available online at www.sciencedirect.com Veterinary Microbiology 133 (2009) 115–122 Usage of antimicrobials and occurrence of antimicrobial a National Veterinary Institute, Technical University of Denmark, Hangøvej 2, Aarhus N DK-8200, Denmark b University of Copenhagen, Faculty of Life Sciences, Department of Veterinary Pathobiology, Stigbøjlen 7, Frederiksberg C DK-1870, Denmark c National Food Institute, Technical University of Denmark, Mørkhøj Bygade 19, Søborg DK-2860, Denmark Received 7 February 2008; received in revised form 2 June 2008; accepted 4 June 2008 The usage of antimicrobials for treatment of mink and the occurrence of antimicrobial resistance among the most important bacterial pathogens in mink was investigated. The aim of the study was to provide data, which may serve as a basis for theformulation of recommendations for prudent use of antimicrobials for mink. A total of 164 haemolytic staphylococci, 49haemolytic streptococci, 39 Pseudomonas aeruginosa, 13 Pasteurella multocida, and 1093 Escherichia coli isolates fromDanish mink were included in the study. A high frequency of resistance among S. intermedius was found for tetracyclines(54.7%), followed by penicillin (21.7%), lincosamides (20.4%), macrolides (19.1%), and spectinomycin (18.5%). Very lowfrequencies of resistance were recorded for other antimicrobials. The highest frequency among the E. coli isolates was recordedfor ampicillin, streptomycin, sulphonamides, and tetracyclines, whereas resistance to other antimicrobials was rare. All P.
aeruginosa were sensitive to gentamicin and colistin and sensitive or intermediate to enrofloxacin, whereas most isolates wereresistant to all other antimicrobials. All P. multocida and haemolytic streptococci were sensitive to penicillin.
There was a steady increase in the use of antimicrobials during the period 2001–2006, the majority of the prescribed amount being extended spectrum penicillins followed by aminoglycosides, sulphonamides with trimethoprim, and macrolides.
# 2008 Elsevier B.V. All rights reserved.
Keywords: Fur animals; Mink; Antibiotics; Antimicrobial resistance; Treatment Mink may suffer from a number of infectious diseases, which demand therapy. The most important * Corresponding author at: KU/LIFE, Department of Veterinary bacterial infections include Escherichia coli (enteritis, Pathobiology, Stigbøjlen 7, DK-1870 Frederiksberg C, Denmark.
pneumonia, septicaemia), Pseudomonas aeruginosa Tel.: +45 35 33 27 03; fax: +45 35 33 27 55.
(haemorrhagic pneumonia), haemolytic staphylo- 0378-1135/$ – see front matter # 2008 Elsevier B.V. All rights reserved.
K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 cocci, most often Staphylococcus intermedius and derived from a variety of samples: skin, intestine or occasionally Staphylococcus aureus (mastitis, pneu- faeces, the urogenital tract, lung, brain, abscesses, monia, pleuritis, dermatitis, metritis, urinary tract pleural cavity, mammary glands, spleen or liver. The E.
infection, septicaemia, and others), Pasteurella mul- coli isolates included in this investigation (n = 1093) tocida (respiratory tract infection, pleuritis, wound were obtained from the intestinal tract, including infection, and others), haemolytic streptococci, mostly faeces, from the urogenital organs, mammary glands, Lancefield’s group G and less frequently group C lungs, liver, or spleen. When E. coli was isolated from (respiratory tract infection, pleuritis, dermatitis, internal organs, they were assumed to be causative wound infection, septicaemia, and others). Other organisms, whereas isolates from the intestine or from bacterial infections occur occasionally, such as faeces could not with certainty be concluded to be infections caused by Salmonella, Plesiomonas shi- causative agents, as E. coli is also a natural inhabitant of gelloides, Streptococcus bovis, Streptococcus pneu- the intestinal tract. The haemolytic streptococci moniae, Aeromonas spp., and others. Although viral (n = 49) belonged to Lancefield’s group G (Strepto- infections cannot be treated with antibiotics, it is not coccus canis) (n = 35) or C (Streptococcus dysgalactiae unusual that such treatment is initiated in an attempt to subsp. equisimilis or Streptococcus equi subsp.
reduce mortality due to secondary bacterial infections zooepidemicus) (n = 14) were derived from a variety to specific viral diseases, such as mink virus enteritis, of sites including the respiratory tract and pleural cavity, distemper, and ‘‘sticky kits’’. An increase in the skin, mammary glands, urogenital system, or from liver prescription of antimicrobials for fur animals has been or spleen in case of septicaemia. The Pseudomonas noted from 659 kg active compound in 2001 to aeruginosa isolates included in the study (n = 39) were all derived from cases of haemorrhagic pneumonia. The same period also an increase in production. So far, few Pasteurella multocida isolates (n = 13) were derived investigations have been carried out on antimicrobial from a variety of sites, but mainly from the respiratory resistance in bacteria from fur animals and the current tract. Primary cultures were made on blood agar (blood knowledge of antimicrobial resistance in important agar base, OXOID, supplemented with 5% calf blood), bacterial pathogens in mink is sparse. The present investigation was undertaken in order to elucidate the medium (Statens Serum Institut, Copenhagen, Den- occurrence of antimicrobial resistance among impor- mark) and subcultured on blood agar. All media were tant bacteria from infections in mink, and to present incubated aerobically at 37 8C for 18–24 h. Bacteria data on the consumption of antimicrobials in mink in were identified from their appearance on agar media, haemolysis, odour, cell morphology, catalase andoxidase reaction and Gram properties. Rapid identifica-tion kits were used as necessary (API ID 32E for E. coli and, API 20NE for P. aeruginosa and P. multocida, APIID 32 STAPH for S. intermedius, and API rapid ID 32 2.1. Bacterial isolates and culture conditions STREP for streptococci, bioMe´rieux, Marcy l’E France). Identification of haemolytic streptococci was Bacterial isolates were obtained from clinical supplemented with a test for positive reaction with samples submitted to the National Veterinary Labora- Lancefield’s group G or C antiserum (OXOID tory during the period 2000–2005. The isolates Diagnostic Reagents), and identification of S. inter- originated from more than 870 mink farms in medius and S. aureus with a positive test for coagulase Denmark and the number of isolates from each farm and a negative and positive test, respectively, for varied from 1 to 11, the majority of farms being represented by 1–4 isolates of different bacterialspecies. Therefore, the isolates were considered 2.2. Antimicrobial susceptibility testing representative for the whole country.
The haemolytic staphylococci (n = 164), of which A semi-automated antimicrobial sensitivity testing 157 were S. intermedius and 7 were S. aureus were system (Sensititre, Trek Diagnostic Systems, East K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 Grinstead, UK), based on the broth dilution method, was used together with customised ready-to-use Antimicrobial resistance among haemolytic staphylococci fromDanish mink microtitre plates containing two-fold dilution amountsof antimicrobials. Different panels were used for different bacterial species. MIC breakpoints were as The usage of antimicrobials for fur animals was based on data extracted from the Danish database on veterinary prescriptions of antimicrobials, VetStat. The prescription of specific antimicrobials for treatment of specific infectious diseases was sought elucidated through a survey among practicing veterinarians.
a Kanamycin: for S. intermedius n = 57 and for S. aureus n = 3.
Significance tests for differences between propor- tions of resistant isolates were calculated usingStatCal in Epi-InfoTM version 6 or SigmaStat version Resistance among E. coli isolates was highest for 3.0. A significance level of 5% was applied ampicillin, streptomycin, sulphonamides, and tetra- ( p < 0.05). Fisher’s exact test (2-tailed) was used cycline. ) whereas very low frequencies of resistance (<5%) were recorded to fluoroquinolones,gentamicin, florfenicol, amoxicillin with clavulanicacid, ceftiofur, chloramphenicol, colistin, nalidixic acid, and apramycin. Among isolates that wereresistant to ampicillin, a significantly higher propor- tion were also resistant to tetracycline than amongampicillin No S. intermedius isolate showed resistance to ( p < 0.001). Similar connections were recorded for amoxicillin with clavulanic acid or fluoroquinolones, ampicillin and sulphonamides ( p < 0.001), ampicillin and resistance was also low for fusidic acid, and trimethoprim ( p < 0.001), tetracycline and cephalothin, kanamycin, potentiated sulphonamides, sulphonamides ( p < 0.001), tetracycline and tri- methoprim ( p < 0.001), and sulphonamides and frequency of resistance was recorded for tetracycline trimethoprim ( p < 0.001). Haemolytic isolates were with 54.7% of the isolates, while resistance to generally more often resistant than non-haemolytic penicillin, macrolides, lincosamides and spectinomy- ones (data not shown), but the differences were only cin was around 20%. The S. aureus isolates were statistically significant for ampicillin, streptomycin, sulphonamides, and tetracycline ( p < 0.001 in all ( p = 0.009) and spectinomycin ( p = 0.030) compared cases). Some differences in resistance patterns to the S. intermedius isolates. Among isolates that between isolates from different origins were observed.
were resistant to tetracycline, a significantly higher Non-haemolytic isolates from the lungs were sig- proportion were also resistant to clindamycin than nificantly more often resistant to streptomycin among tetracycline sensitive isolates, and vice versa, ( p = 0.041) and trimethoprim ( p = 0.009) than iso- ( p = 0.04). A similar correlation was recorded for lates from faeces or intestines, and were also clindamycin and penicillin ( p = 0.002).
significantly more often resistant to trimethoprim K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 Table 2Antimicrobial resistance of E. coli isolates from Danish mink a Cephalothin: for faeces or intestine n = 462, for lungs n = 155, for spleen or liver n = 115, for urogenital tract or mammary glands n = 20, for ( p = 0.002) than isolates from the spleen or liver. For mides with trimethoprim. The highest frequency of haemolytic isolates, frequencies of resistance to resistance was recorded for clindamycin and ery- ampicillin ( p = 0.017) were significantly higher in isolates from the urogenital tract or mammary glands Although a difference was noticed for tetracycline than in isolates from faeces or intestine.
in resistance between group G (17.1%) and C (42.9%) All P. aeruginosa isolates were sensitive to isolates, this difference was not statistically signifi- gentamicin and colistin and only 5.1% of the isolates were resistant to enrofloxacin. In contrast, all isolateswere resistant to ampicillin, amoxicillin with clavu-lanic acid, cefalothin, chloramphenicol, lincosamides, macrolides, and spectinomycin and most isolates were Antimicrobial resistance of haemolytic streptococci (n = 49) from P. multocida isolates were invariably sensitive to penicillin and ampicillin, chloramphenicol, gentami- cin, colistin, spectinomycin, tetracycline, sulphona- mides with trimethoprim, cefalothin, enrofloxacin and kanamycin. In contrast, all isolates were resistant or intermediately sensitive to erythromycin and clinda- mycin, the majority being resistant (61.5% and 92.3%, Isolates of haemolytic streptococci were all sensitive to penicillin, cephalothin, and sulphona- K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 Table 4Antimicrobials (kg active compound) sold for use in fur animals in Denmark during the period 2001–2006 resistance to tetracycline was considerably higher,54.7% in mink compared to 23.9% in dogs. The The usage of antimicrobials for mink in Denmark differences for fusidic acid can be explained by the during the period 2001–2006 is recorded in fact that this compound is never used for mink, but often in dogs for treatment of skin-, ear-, and eye has been a steady increase in usage every year during infections. Explanations for the differences observed this period. The increase was noted for all anti- for penicillins and tetracyclines are less obvious but they may be due to usage patterns or to co-selection asthere seemed to be some correlation in resistancebetween certain antimicrobials. Thus, there was a significantly higher proportion of tetracycline resistantisolates that were also resistant to clindamycin than among tetracycline sensitive isolates, and vice versa,and similar for clindamycin and penicillin. Any S. intermedius is mostly associated with mink, dogs genetic background for these correlations is not known and other carnivores, and is one of the most commonly but deserves to be investigated. A small number of S.
isolated pathogenic bacteria in these animals. This intermedius and S. aureus isolates were found to be bacterial species is involved in a plethora of infectious resistant to cephalothin although they were sensitive to conditions in mink, such as pneumonia and pleuritis, amoxycillin with clavulanic acid. This may seem dermatitis, urinary tract infections, metritis, and contradictory, but is likely to be a methodolic problem, mastitis. Reliable data for comparison only exist for i.e. MIC values close to the breakpoints, or similar.
dogs and to a lesser extent cats. There was The resistance patterns for the S. aureus isolates considerable difference between antimicrobial resis- seemed different from those of S. intermedius from tance of S. intermedius from mink compared to canine both mink and dogs (), although the differences were only statistically significant for few antimicro- The frequency of resistance was much lower to bials. This may indicate a different origin of the S.
penicillin, 21.7% of the mink isolates compared to aureus. Thus, S. intermedius is closely connected with 60.2% in dogs, and fusidic acid, 3.8% in mink mink and other carnivores, and the infections are compared to 30.9% in dogs, whereas the frequency of therefore possibly caused by strains from the mink K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 themselves, whereas the infections with S. aureus may 33.1% of the haemolytic isolates and 20.9% of the have been acquired from other sources. S. aureus is non-haemolytic isolates resistant to tetracycline. In an often associated with cattle, poultry, and humans and investigation of E. coli from clinical submissions, although a certain host specificity of different S.
resistance frequencies among isolates from cattle and aureus clones has been recorded, transmission pigs were 91% and 72%, respectively, to tetracycline, 93% and 37% to ampicillin, 85% and 75% to However, clonality studies of staphylococci from sulphonamides, and 54% and 31% to trimethoprim mink have not been carried out, and thus, the origin and transmission of strains is not well elucidated.
are higher than those found in the present study.
We found no haemolytic streptococci resistant to demonstrated considerable differences in antimicro- penicillins, cephalosporins or sulphonamides with bial resistance of E. coli between different farms. The trimethoprim. A high frequency of resistance was present study included isolates from a large number of recorded for tetracycline, in particular among the farms but usually only one isolate from each farm, and group C isolates, although tetracyclines, as previously the figures do therefore not allow for comparison mentioned, are not extensively used for mink. The between farms, nor do they allow for calculations as to highest resistance was recorded to lincosamides and whether a high frequency of resistance to certain macrolides, both with 68.6% resistance among the antimicrobials on a farm in one bacterial species also group G streptococci. This is much higher than leads to high frequency of resistance in other bacterial recorded for group G streptococci from dogs isolated during the same period (15.5% and 10.8%, respec- The relatively high level of resistance to tetra- cyclines may seem surprising as tetracyclines are clear, but may be explained by the frequent use of rarely used in the mink production, and has not been tylosin or lincospectin for mink, whereas macrolides used to any significant extent during resent years. The and lincosamides account for a smaller fraction of the connection between resistance to tetracyclines and S. canis (group G) is almost restricted to sulphonamides and in the present investigation, we carnivores and resistance data are only available from also demonstrated significant correlations between dogs – and now from mink – whereas group C resistance factors. Thus, among isolates that were streptococci cause infections in many animal species, resistant to ampicillin, a significantly higher propor- tion were also resistant to tetracycline than among P. multocida is a common causative agent of ampicillin sensitive isolates, and vice versa, and infections of the respiratory tract, the urogenital tract similar correlations were recorded between ampicillin and skin infections in several animal species. We and sulphonamides, ampicillin and trimethoprim, found all isolates sensitive to all antimicrobials, except tetracycline and sulphonamides, tetracycline and for macrolides and lincosamides, to which all isolates trimethoprim, and sulphonamides and trimethoprim.
were resistant or intermediate sensitive. This is in The genetic background for these correlations is accordance with a recent observation on isolates from unknown but the phenomenon deserves further investigation as genetic linkages may very well lead investigations on P. multocida from pigs to co-selection of resistance and thereby maintenance of a high frequency of resistance to certain anti- microbials, even if they are not used for treatment.
that isolates were susceptible to penicillins, cepha- Investigations of antimicrobial resistance among E.
losporins, aminoglycosides, tetracyclines, and fluor- coli isolates from Denmark have shown marked oquinolones, whereas results for macrolides and and frequencies of resistance among indicator E. coli reported resistance to tylosin but sensitivity to are considerably lower than those among pathogenic erythromycin, something which is not very likely. This E. coli isolates. In the present investigation, we found is probably a methodological problem.
K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 From a veterinary point of view, P. aeruginosa is penicillins with 302 kg, but in terms of percent it often involved in chronic otitis externa in dog and it is was potentiated sulphonamides with 275 kg or 833%.
the causative agent of haemorrhagic pneumonia in The increase has been highest on compounds for which mink. Apart from these conditions, this bacterial agent the dosage per animal is high, and this makes the is usually only a sporadic pathogen in animals, such as increase seem more dramatic. The most used anti- in septicaemia in chickens or bovine mastitis. P.
microbials were extended spectrum penicillins, mainly aeruginosa is reputed for its innate resistance to most amoxicillin. An unofficial survey among Danish veterinarians working with fur animals, indicated that sensitivity was only found for two antimicrobials in amoxicillin was used for treatment of a number of this investigation: colistin and gentamicin. For enro- infectious diseases, i.e. ‘‘sticky kits’’, diarrhoea, urinary floxacin, only 5.1% of the isolates were resistant, but for tract infections, pneumonia, pleuritis, and abscesses.
most other antimicrobials, most or all isolates were The second most used antimicrobials were aminoglyco- resistant. It should be mentioned, though, that 18 of 39 sides; this seemed to be mostly apramycin and isolated showed intermediate susceptibility to enro- neomycin, which was used for treatment of diarrhoea.
floxacin, indicating that the MIC values of this Sulphonamides with trimethoprim came up third.
bacterium lie close to the breakpoints. In a study of Potentiated sulphonamides, which was sulphadiazine P. aeruginosa from Danish dogs, 35.9% were found to with trimethoprim available from various companies, be resistant to enrofloxacin, and low levels of resistance both for oral and parenteral application, were used were also noted for colistin (2.56%) and gentamicin against a broad spectrum of diseases, e.g. diarrhoea, (15.4%). These differences may be related to the use of urinary tract infections, and pneumonia (P. aeruginosa- gentamicin and polymyxins for treatment of ear associated). Sulphonamides with trimethoprim are the infections in dogs. Considering the results of the drug of choice for treatment of haemorrhagic pneu- sensitivity testing it is surprising that practicing monia caused by P. aeruginosa. The fourth most used veterinarians often prescribe vaccination in combina- antimicrobials were macrolides, almost exclusively tion with treatment with potentiated sulphonamides tylosin, which was mostly used for sticky kits.
during outbreaks of haemorrhagic pneumonia. In spite Lincosamides and tetracyclines were less often used, of the lack of in vitro susceptibility, these antimicrobials but in similar amounts. Lincosamides were mainly used are reported clinically to limit the course of an outbreak.
in the form of lincospectin. This was used for a numberof infectious diseases, e.g. ‘‘sticky kits’’, diarrhoea, pneumonia, and pleuritis. Tetracyclines were used fortreatment of ‘‘sticky kits’’, pneumonia (not P.
Use of antimicrobials in mink (and all other aeruginosa-associated), and maybe other infections.
animals) in Denmark is based on veterinary prescrip- Other antimicrobials were used only in negligible tion only. This would prevent misuse or overuse of antimicrobials, as it must be assumed that allantimicrobial use in mink is based on needs deemed by a veterinary practitioner. The usage of antimicro-bials for fur animals during the period 2001–2006 is Very few investigations on antimicrobial resistance listed in . There has been a steady increase in among bacteria from mink have been carried out. A consumption during this period, which may be explained by an increase in production and increased few isolates of each bacterial species to draw problems with specific disease problems, in particular meaningful conclusions, and included a number of haemorrhagic pneumonia caused by P. aeruginosa, bacterial species that were irrelevant from a ther- distemper, mink virus enteritis, and ‘‘sticky kits’’. The apeutic point of view. Thus, the present study is, to our increase in usage was recorded for all major classes of knowledge, the first thorough investigation of the antimicrobials. From 2001 to 2006 the total increase occurrence of antimicrobial resistance among impor- was 1035 kg corresponding to 157%. The highest tant bacterial pathogens from mink and the usage of increase in terms of kg active compound was antimicrobials for fur animals. Valid comparison of K. Pedersen et al. / Veterinary Microbiology 133 (2009) 115–122 the amounts of antimicrobials used in mink in animals, foods and humans in Denmark. Copenhagen, Denmark, Denmark and other countries is difficult, as few Anon., 2007. DANMAP 2006—Use of antimicrobial agents and countries have comparable production regimes and occurrence of antimicrobial resistance in bacteria from food consumption data is sparse. Our data on antimicrobial animals, foods and humans in Denmark. Copenhagen, Denmark, resistance and usage of antimicrobials are therefore mainly descriptive, and do hardly allow conclusions to Fales, W.H., Turk, J.R., Miller, M.A., Bean-Knudsen, C., Nelson, be drawn as to the appropriateness of resistance and S.L., Morehouse, L.G., Gosser, H.S., 1990. Antimicrobial sus-ceptibility of Pasteurella multocida type D from Missouri swine.
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occurrence of antimicrobial resistance in bacteria from food

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