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* Clinic for Reproduction, Faculty of Veterinary Medicine, Free University of Berlin, Koenigsweg 65, D-14163 Berlin, Germany
Federal Office of Consumer Protection and Food Safety (BVL), Diedersdorfer Weg 1, D-12277 Berlin, Germany
1 Corresponding author: author{at}bestandsbetreuung.de
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Key Words: dairy cow • mastitis • antimicrobial resistance
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Resistance of mastitis pathogens to antimicrobial agents is a well-documented challenge in dairy cows (Owens et al., 1997; Lotthammer and Klarmann, 1999; Trolldenier, 1999; Erskine et al., 2002; Makovec and Ruegg, 2003b; Pitkala et al., 2004). The World Health Organization (WHO) has stated that any use of antimicrobial agents is associated with the risk of inducing resistance to antimicrobial agents among bacteria (WHO, 1997). This has called for more investigations into the use of antimicrobial agents in food-producing animals and the determination of potential factors that influence the level of resistance in mastitis pathogens (Lotthammer and Klarmann, 1999; Osteras et al., 1999; Trolldenier, 1999; Aarestrup, 2005). Regional differences in resistance patterns of pathogens exist in Germany and worldwide (Salmon et al., 1998; Lotthammer and Klarmann, 1999; de Oliveira et al., 2000). However, a relationship between the resistance patterns of mastitis pathogens and the intensity of food animal husbandry in the respective regions could not be established (Lotthammer and Klarmann, 1999; Schröter, 2003).
Differences in resistance patterns between reports may be caused to some extent by the variation in methods used for the determination of resistance against antimicrobial agents. Early reports on resistance, but also some recent ones (Erskine et al., 2002; Makovec and Ruegg, 2003b) were based on the disk diffusion method, which has been shown not to correlate well with the minimum inhibitory concentrations (MIC) determined by dilution methods (Kibsey et al., 1994; Kelly et al., 1999). Presently, dilution methods are recommended by expert groups as the methods of choice (Erskine et al., 2004; Luhofer et al., 2004).
Resistance of Staphylococcus aureus to penicillin or ampicillin has been extensively studied (Erskine et al., 2004). Although the MIC of penicillin against Staph. aureus did not differ between strains isolated from heifers and cows in one study (Watts et al., 1995), a recent report has demonstrated numerically higher proportions of penicillin-resistant CNS in older cows compared with isolates from primiparous cows (Rajala-Schultz et al., 2004). Treatment with penicillin at dry off has been proposed to exert selection pressure toward penicillin-resistant Staph. aureus strains (Osteras et al., 1999).
Resistance to antimicrobial agents in mastitis pathogens has 2 relevant aspects: The first is a reduction in cure rates after treatment of clinical mastitis cases (Owens et al., 1997; Sol et al., 2000). The second issue is the potential impact of transmission of resistant bacteria to humans via the food chain (Ungemach, 1999). This is not likely to occur with milk from clinical cases of mastitis, because this milk is banned from human consumption. However, clinical cases may turn into subclinical cases or latent infections. Resistant bacteria from these infections are present in the bulk tank milk and may therefore be transmitted to humans via raw milk products.
In eastern German provinces, herd sizes are bigger than in most other parts of the European Union. Limited literature exists on the contribution of different mastitis pathogens to the mastitis problem of these dairy herds and on their management practices concerning mastitis problems.
Therefore, the objectives of this study were to determine management practices concerning mastitis, and the prevalence of mastitis pathogens in clinically healthy quarters of dairy cows in Brandenburg, Germany. A further objective was to determine the susceptibility of these bacteria to 6 antimicrobial agents that are or have been commonly used in dairy cows. Finally, we investigated whether the prevalence of ampicillin resistance of Staph. aureus was influenced by parity or stage of lactation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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All farms were visited once between July 2001 and October 2002 by the same investigator. Management practices, housing conditions, and milking routines were evaluated and documented on a standardized data capture form. Milking routines were recorded by observation of routine milking over one milking period. Management of cows with mastitis was recorded as observed during the visit. For events that could not be observed during the visit (e.g., dry-cow routines, treatment protocols), management was recorded as indicated by the farm manager in a questionnaire covering 20 items.
Aseptic quarter foremilk samples were collected from 4 groups of animals: 1) Primiparous cows at the beginning of the lactation (
50 DIM); 2) primiparous cows at the end of lactation (
250 DIM); 3) older cows ( second lactation) at the beginning of the lactation (50 DIM); and 4) older cows ( second lactation) at the end of lactation (250 DIM).
Eight clinically healthy cows of each of the 4 groups were sampled at milking time before cluster attachment on each farm. Cows were selected in order of their appearance in the milking parlor during the visit. Cows with blind quarters were included, but they only contributed 3 samples per cow (Table 1
). Samples were cooled and shipped to the laboratory at the same day.
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Determination of the MIC
The MIC of the bacteria was determined using the microbroth dilution method in accordance with instructions M31-A2 of the Clinical Laboratory Standards Institute (CLSI, 2002). The evaluation was undertaken visually with the help of a semiautomatic readout device (SensiTouch, MCS Diagnostics, Swalmen, The Netherlands). To validate the results obtained, the bacterial counts of the bacterial suspension and the purity of the inoculum were determined. Reference strains Staph. aureus ATCC 29213 and Escherichia coli ATCC 25922 (Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH; Brauschweig, Germany) were examined in parallel. The MIC level was defined as the minimum concentration of an antimicrobial agent that inhibited visible growth.
Minimum inhibitory concentrations of 6 antimicrobial agents (ampicillin, oxacillin, amoxicillin/clavulanate, gentamicin, cefquinome, and streptomycin) were determined for the gram-positive pathogens Staph. aureus (n = 199), Strep. uberis (n = 69), Strep. dysgalactiae (n = 30), and Enterococci (n = 27) using commercial microtiter plates. Streptococcus agalactiae was not tested because it was assumed to be generally susceptible to penicillin.
Statistical Analyses
The association of IMI with group was tested using logistic regression with group (1 to 4), quarter (1 to 4), and herd as categorical covariates and the presence of the respective pathogen as binary outcome. Logistic regression was run twice for each pathogen with 2 reference groups for the covariate group; i.e., group 1 and group 4. This was done to be able to better identify the effects of parity and stage of lactation. Only pathogens that were isolated from a minimum of 50 quarters were selected as outcome variables. Separate models for the different pathogens were calculated with quarters that carried a pathogen different from the outcome pathogen being coded as not infected with the pathogen in question. Blind quarters and samples that could not be analyzed were coded as missing values.
To control for possible interactions between the quarters of individual cows, the same analysis was performed on the cow level. Cows were coded as positive for a respective pathogen, if at least one quarter was infected with the pathogen, otherwise negative.
In addition to the analysis by pathogen, a ratio between major contagious and environmental pathogens was calculated to summarize the contribution of environmental and contagious pathogens to the infection pattern of the 4 groups. Contagious pathogens in this calculation were Staph. aureus and Strep. agalactiae. Environmental pathogens were all Streptococcus spp. (except Strep. agalactiae), all enterococci, and coliforms.
The association of group with Staph. aureus resistance to ampicillin was tested using binary logistic regression with resistance to the antimicrobial agent as the binary outcome and group, herd, and quarter as covariates. The analysis was carried out for 2 different breakpoints (0.25 and 0.5 mg/L) to account for different breakpoints set in different countries. This analysis was not performed for the other bacteria and for other antimicrobial agents against Staph. aureus, because the number of isolates was limited and variability was low.
All logistic regressions were carried out using SPSS software (SPSS 12.0, SPSS Inc., Munich, Germany).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Management Practices
Cows with clinical cases of mastitis were transferred into a sick cow pen in 56 of the 80 farms. Another 8 farms housed these animals together with other cows producing nonsaleable milk (i.e., fresh cows). Of the 16 farms (20%) that did not separate the sick and treated cows from the producing herd, 2 had their cows in the herd without marking them. They relied on the accuracy of the person in the milking parlor. One herd used the software provided by the milking parlor to block sick cows from the bulk tank. The other 13 herds marked the cows with color bands around the legs.
Results of the questionnaire on mastitis management indicated that in 35% of the farms cephalosporins (cefoperazone and cefquinome) were used as the first choice of treatment for clinical mastitis. Oxacillin or cloxacillin was used on 17% and penicillin was the first choice on 13% of the farms. Oxytetracycline was used on 6% of the farms and fixed commercial combinations of antimicrobial agents were used on 27% of farms. The fixed combinations were variable, but in the majority of cases they contained 1 antimicrobial agent directed against gram-positive and 1 against gram-negative bacteria. Eighteen farms did not give information on the type of product they used. Information on type of treatment (intramammary or systemic) was not requested.
Three or more treatments per case of clinical mastitis were carried out by 47% of the farmers that responded to this question (77 of 80). Information on the interval between treatments was not requested. Three farmers (4%) administered a minimum of 2 treatments. The other farmers treated "until the secretion looked normal again" (47%) or SCC dropped according to California Mastitis Test results (3%).
Nineteen farmers did not report the maximum number of treatments for one case of mastitis. Six farmers performed a therapy "until there was success". Of the farmers with more detailed answers (55 of 80), most (45%) gave a maximum of 3 to 4 treatments. Twelve farmers (22%) treated more and longer, 16 (29%) less often.
Twelve farmers (15%) changed the antimicrobial agent during the treatment of mastitis cases. Seventeen (22%) did not do so and most of the farmers changed the antimicrobial agent from time to time (63%). Two farmers did not answer this question.
Blanket dry-cow therapy was performed on 67 of the 79 farms that provided an answer to this question. Another 12 farmers used dry-cow therapy selectively for cows with high SCC (10 farmers, threshold not specified) or a case of clinical mastitis during lactation (3 herds). Twelve farmers did not provide information about the medicinal products they currently used for dry cows. Cloxacillin alone (46%) or in combination (21%) was the antimicrobial agent most often used at dry-off. Penicillin was used on 31% of the farms and neomycin on 24%. Other antimicrobial agents used for this purpose were framycetin (21% in combination with penicillin), streptomycin and nafcillin (6% in combination with penicillin), cefoperazone, ampicillin, and erythromycin (1% each).
Microbiological Cultures
A total of 9,910 milk samples collected from 2,529 cows were included in the study. For technical reasons (contamination or broken samples), 124 samples (1.2%) of 31 cows could not be included. Two hundred and six quarters (2.0%) were blind.
Of the samples included in the study, 2,614 (26.4%) samples contained mastitis pathogens (Table 1
). Corynebacterium bovis and CNS were the predominant findings, accounting for 62.2% of the positive samples. Among the major pathogens isolated, Staph. aureus was the predominant contagious agent (21.8%) and Strep. uberis (3.7% of the positive samples) was the major environmental pathogen.
Effect of group, herd, and quarter was tested for CNS, C. bovis, Staph. aureus, Strep. uberis, Strep. agalactiae, other streptococci, and negative samples. More samples were negative in primiparous than in older cows (P < 0.001) and in early lactation than in late lactation (P < 0.001). The prevalence of CNS was lower in older than in primiparous cows (P < 0.001), but did not differ between early and late lactation. On the other hand, the prevalence of C. bovis was higher in late lactation (P < 0.001) and in multiparous cows (P < 0.001). The prevalence of Staph. aureus increased during lactation (P < 0.001). In late lactation, it was higher in older cows than in primiparous cows (P < 0.05). Streptococcus agalactiae was more prevalent in older than in primiparous cows in early (P = 0.001) and late lactation (P = 0.05). However, there was no significant effect of stage of lactation on the prevalence. In older cows, the prevalence of Strep. uberis increased during lactation (P = 0.01) and was higher in late lactation than in primiparous cows in late lactation (P < 0.001).
A second analysis, carried out at the cow level to control for possible interactions between the quarters, delivered the same significant differences between the groups with one exception. The difference in prevalence of Strep. uberis between early- and late-lactation multiparous cows was not significant on the cow level.
The overall ratio between contagious major pathogens (Staph. aureus and Strep. agalactiae) and environmental major pathogens (nonagalactiae streptococci, coliforms) was between 1.73 and 2.13 in groups 1, 3, and 4, respectively. In contrast, late-lactation primiparous cows (group 2) showed a ratio of 3.25 indicating a substantial increase in contagious pathogens (4.1 to 6.6%) compared with environmental pathogens (2.2 to 2.1%) during the first lactation. In older cows, the increase in contagious pathogens was within the same range (5.7 to 8.9%), but there was also an increase in environmental pathogens (3.3 to 4.2%).
There was great variation between farms concerning the prevalence of mastitis pathogens. Only CNS were identified in samples from all farms (Table 2).
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). Twenty-five cows contributed 2 isolates. In 19 cases, these were from different species; in 6 cases, they were from the same species. The maximum number of isolates per farm was 10; of these, no more than 8 were from the same species.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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The analysis of factors associated with IMI on the quarter level is always confronted with the complex interrelationship of quarters and the effect of one pathogen on the risk of infection with another. To cope with the first obstacle we chose to perform the analysis on both the quarter and cow levels. The close-to-perfect agreement of the differences between groups indicates that for the purpose of this study, the interaction between quarters of individual cows was of minor importance.
A possible interaction between pathogens was ignored in this study. This seemed reasonable, because we did not study the risk of new infections in cows over time but in different groups of cows. Because about 75% of the quarters were negative, the possible effect of the interaction was probably small.
Besides the minor pathogens, Staph. aureus was still the pathogen with the highest prevalence in clinically healthy animals. This is in accordance with data from other countries (Poelarends et al., 2001; Gianneechini et al., 2002). In our study, the prevalence of Staph. aureus was higher in late than in early lactation. In late lactation, multiparous cows carried more Staph. aureus infections than primiparous cows, whereas the difference in early lactation was not significant. This may be due to the widespread use of dry-cow therapy in the herds studied that is known to reduce the prevalence of Staph. aureus effectively. The higher susceptibility of older cows to IMI with Staph. aureus in the course of lactation is in accordance with a report on a higher susceptibility of quarters that had been infected with Staph. aureus previously (Zadoks et al., 2001), which is more likely in older cows. However, it is not clear whether these are new infections or flare-ups of old infections that were not fully eliminated.
Streptococcus agalactiae was still found in about 30% of the herds. This has also been reported for other European countries (Poelarends et al., 2001). Data from the United States suggest a somewhat higher prevalence of this species. In contrast to 2.7% of our bacteriologically positive samples, Strep. agalactiae was found in 13.1% of the positive samples in New York and Pennsylvania (Wilson et al., 1997) and in 7.7% of the positive samples in Wisconsin (Makovec and Ruegg, 2003a). However, these papers report data from years ago and the samples in these 2 studies were from diagnostic laboratories and likely included more samples from problem herds and problem cows. Makovec and Ruegg (2003a) described a constant decline of the prevalence of Strep. agalactiae in their diagnostic material with a prevalence of 3% in the last year of their investigation, which is similar to our results.
As expected, Strep. uberis had the highest prevalence among the environmental pathogens (Morin et al., 2001; Poelarends et al., 2001). Strep. uberis was more prevalent at the end of lactation in older than in primiparous cows, whereas it did not differ significantly between the age groups in early lactation (Todhunter et al., 1995; Zadoks et al., 2001). In contrast to the prevalence of Staph. aureus, the prevalence of Strep. uberis in primiparous cows did not increase during lactation. This explains the increase of the ratio between contagious and environmental pathogens in primiparous cows at the end of lactation (Zadoks et al., 2001).
Antibiotic Resistance
Data on the amount of antimicrobial agents used in dairy cows and on treatment procedures applied by practitioners and farmers are limited (Grave et al., 1999; DANMAP, 2003) or anecdotal when problems occur that are associated with treatment protocols (Schukken et al., 2000). Although the overall use of antimicrobial agents is lower in dairy cows than it is in the pork or poultry industries (DANMAP, 2003), routine treatments like dry-off therapy are widely recommended and implemented on almost all large farms in Germany. Cephalosporins, penicillins, and synthetic penicillins that are resistant to ß-lactamase account for most of the treatments in the study farms. This is in line with reports from Denmark (DANMAP, 2003).
Comparing the classification of bacteria as susceptible or resistant requires reference to the breakpoints used. For several antimicrobial agents, no generally accepted veterinary breakpoints are available (Kietzmann et al., 2004). Overall, the proportion of isolates that were resistant to the antimicrobial agents tested was within the range of other reports from Germany using the same breakpoints (Trolldenier and Wagner, 2001; Schröter, 2003; Wallmann et al., 2003, 2004). Reports based on the agar gel-diffusion method are difficult to compare with those performed with dilution methods because there is only limited agreement between the results of the 2 methods (Kibsey et al., 1994; Kelly et al., 1999, Schwarz et al., 2003).
Enterococci.
Enterococcus spp. are frequently used as indicator bacteria for the development of antimicrobial resistance (DANMAP, 2003). Limited information is available from random samples of bacteria in dairy cows, and even less on mastitis pathogens isolated from milk samples (Rossitto et al., 2002; Pitkala et al., 2004). The susceptibility data of the examined enterococci showed no resistance to ampicillin (breakpoint 8 mg/L). This result and the MIC90 of 1 mg/L correspond with data from other reports (Watts et al., 1995; Rossitto et al., 2002; Schlegelova et al., 2002). The MIC90 of oxacillin and cefquinome for enterococci were high in our study (64 and 8 mg/L, respectively). Resistance to oxacillin and cephalosporins is common among enterococci (Watts et al., 1995; Myllys et al., 1998; Rossitto et al., 2002; Schlegelova et al., 2002). The MIC90 of streptomycin was lower than in other reports (Schlegelova et al., 2002; DANMAP, 2003).
Staphylococcus aureus.
In our study, the MIC90 of ampicillin for Staph. aureus isolates was higher than in other studies (Salmon et al., 1998; Schröter, 2003; Wallmann et al., 2004) but in agreement with an international study (de Oliviera et al., 2000). Some authors reported a reduction in the proportion of Staph. aureus isolates that were resistant to ß-lactams over the last decade when the disk diffusion method was used (Erskine et al., 2002; Makovec and Ruegg, 2003b). Salmon et al. (1998) reported striking differences in the efficacy of penicillin and cephalosporins against Staph. aureus isolates isolated from heifers in New Zealand and Denmark.
The MIC90 of oxacillin for Staph. aureus was in the same range as in most other studies (de Oliveira et al., 2000; Gentilini et al., 2000; Yoshimura et al., 2002; Schröter, 2003). The MIC90 of streptomycin for Staph. aureus was lower than in a recent report from the Czech Republic (Schlegelova et al., 2002), but slightly higher than the 2 mg/L reported from a German survey (Schröter, 2003). For gentamicin, the MIC90 of 0.5 mg/L underlines the results of other recent studies (Yoshimura et al., 2002; Schröter, 2003; Wallmann et al., 2004).
Information on the susceptibility of Staph. aureus from milk to amoxicillin/clavulanic acid is rare in the literature. The MIC90 of 1 mg/L determined in this study is similar to other recent German studies (Schröter, 2003; Wallmann et al., 2004) but higher than published for Germany in an international study (de Oliveira et al., 2000).
Streptococcus uberis.
All Strep. uberis isolates were susceptible to ampicillin, amoxicillin/clavulanic acid, and cefquinome according to breakpoints published by Clinical Laboratory Standards Institute (CLSI, 2002). This supports data from several other reports (Owens et al., 1997; Trolldenier, 1999; Rossitto et al., 2002; Pitkala et al., 2004). The MIC90 of 2 mg/L for oxacillin was within the range of other studies. In an older German study, Trolldenier (1999) also determined a MIC90 of 2 mg/L. Rossitto et al. (2002) reported a slightly lower MIC90 of 1 mg/L for milk samples from California. Salmon et al. (1998) reported 16 mg/L, but they only tested 15 isolates from Denmark.
Streptococcus dysgalactiae.
Minimum inhibitory concentrations of ampicillin and cefquinome were low for Strep. dysgalactiae. Rossitto et al. (2002) reported a MIC90 of 0.06 mg/mL of ampicillin for 152 isolates of Strep. dysgalactiae; they did not test lower concentrations. In our study, we found 0.03 mg/L to be inhibitory as well. Likewise, the MIC90 of 0.125 mg/L determined for oxacillin in our study is below the tested concentration in the study reported by Rossitto et al. (2002). Trolldenier (1999) reported an MIC90 of 0.016 mg/L for ampicillin and 0.09 mg/L for oxacillin.
Factors Affecting Antibiotic Resistance.
The proportion of ampicillin-resistant Staph. aureus isolates was significantly lower in primiparous cows in early lactation than in the same age group in late lactation. To our knowledge, this difference has not been described before. Recently, Rajala-Schultz et al. (2004) reported a numerical difference in the proportion of penicillin-resistant CNS between primiparous and older cows. Drying off with antimicrobial drugs designed for lactation therapy has been proposed as a risk factor for subclinical mastitis with penicillin-resistant Staph. aureus strains (Osteras et al., 1999). Although a difference between age groups may have been caused by dry cow therapy selectively eliminating the strains susceptible to penicillin, this cannot explain the difference between early and late lactation in primiparous cows.
It has been proposed that strains susceptible to penicillin are also more susceptible to lactation therapy (Sol et al., 2000). This may be a selective pressure during lactation; however, treatment records of the cows that were sampled were not available.
Another possible explanation is the genetic diversity of strains found in early lactation primiparous cows and in older cows. Recently, it has been demonstrated that in herds with good milking hygiene, sporadic IMI with Staph. aureus are caused by a variety of strains even in the same herd, indicating an environmental origin of the strains (Sommerhäuser et al., 2003). In herds with poor milking hygiene, strains were more homogeneous. Infections present in primiparous cows at the onset of lactation are likely to be of environmental origin too, because these animals have not been confronted with the milking process. Sommerhäuser et al. (2003) have proposed that these strains might also be less adapted to the mammary gland and therefore be more easily eliminated and less easily spread within the herd. With respect to the results of our study this may be a cause of the increasing proportion of ampicillin resistant isolates not related to use of antimicrobial agents but to the ecology of the respective Staph. aureus strains. Further research will be needed to investigate this hypothesis.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Antimicrobial resistance determined in our study was in line with other reports. Interestingly, a lower proportion of ampicillin-resistant isolates of Staph. aureus was found in early lactation primiparous cows. This finding indicates the need for further investigation of the epidemiology of resistance against penicillin in Staph. aureus isolated from bovine mammary glands.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Received for publication October 26, 2005. Accepted for publication February 6, 2006.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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