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* University of Guelph, Guelph, Ontario N1G 2W1, Canada
Quality Milk Promotion Services, Cornell Univesity, Ithaca New York 14850-1263 USA
University of Montreal, St. Hyacinthe, Quebec J2S 7C6 Canada
University of Prince Edward Island, Charlottetown, P.E.I. C1A 4P3 Canada
|| Tavistock Veterinarians, 25 Hope St. East Tavistock, Ontario, N0B 2R0
# Provel, Division of Eli Lilly Canada Inc., Research Park Centre, Guelph, Ontario N1G 4T2 Canada
Corresponding author:
R. T. Dingwell; e-mail:
rdingwell{at}vet.k-state.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Key Words: Staphylococcus aureus • dry cow therapy • tilmicosin
Abbreviation key: CNS = coagulase-negative staphylococci, CP5 = capsular polysaccharide 5, DCT = dry cow antibiotic therapy, LS = linear score, OR = odds ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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With very few exceptions, cure of major mastitis pathogens following DCT is not likely a random event. Variation in cure rate may be explained by pathogen, cow, and herd factors. It would be of considerable importance to the dairy industry to be able to predict which cows were more likely to cure (Schukken et al., 2001). In an attempt to augment the effectiveness of DCT, various protocols and products have been tested (Soback et al., 1990; Hogan et al., 1995; Erskine et al., 1998; Nickerson et al., 1999). One such treatment that has recently been investigated is the use of tilmicosin.
Tilmicosin is a semisynthetic macrolide antibiotic, currently approved for the treatment of bovine respiratory disease. This drug possesses properties that might prove favorable in combatting dry period IMI, especially subclinical S. aureus infections. These properties include the observed in vitro interactions of the antibiotic with bovine phagocytes and epithelial cells (Scorneaux and Shryock, 1999). Tilmicosin is rapidly accumulated in bovine macrophages and mammary epithelial cells. The uptake in mammary gland cells is dependent on cell viability, temperature, and pH, but is not influenced by either metabolic inhibitors or an anaerobic environment (Scorneaux and Shryock, 1999).
In recently published research, tilmicosin was compared to intramammary cephapirin benzathine as a treatment of S. aureus at dry-off (Nickerson et al., 1999). The tilmicosin was either administered intramammary (1500 mg) or via a subcutaneous injection at 5 mg/kg of BW on the day of drying-off, and again 4 d later. The reported quarter cure rates for IMI caused by S. aureus at 28 d post calving were: 78.1% intramammary cephapirin, 74.2% intramammary tilmicosin, and 9.1% subcutaneous tilmicosin. Intramammary tilmicosin was concluded to be as effective as cephapirin benzathine.
In addition to new treatment regimes, considerable attention has been concentrated on identifying specific risk factors that influence the cure of S. aureus, such that DCT might be specifically aimed at only those cows with a high probability of cure (Sol et al., 1994). This implies that a manager would have to decide to remove cows from the herd that have a low probability of cure. There are significant quarter level and cow level predictors for cure of S. aureus. Cure rate has been shown to be strongly influenced by the location of the infected quarter in either the front of the hind of the udder, the age of the cow, the percentage of samples that were culture positive for S. aureus before drying-off, the SCC of infected quarters and the total number of quarters that are infected (Sol et al., 1994; Osteras et al., 1999).
The efficacy of intramammary tilmicosin to eliminate S. aureus has recently been reported from data collected in two herds, with the majority of cows having experimental infections (Nickerson et al., 1999). The objective of this paper is to present the results of a DCT field trial that evaluated the efficacy of intramammary tilmicosin phosphate to eliminate naturally occurring S. aureus, and identified risk factors associated with achieving cure of subclinical S. aureus IMI during the dry period.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Sampling Time Line and Treatment Randomization
A study technician collected quarter milk samples aseptically from all eligible cows starting between 28 (d -28) and 22 (d -22) d before scheduled drying-off, and again between 21 (d -21) and 14 (d -14) d before drying-off. Drying-off date was calculated to ensure cows would have a minimum 60-d dry period for residue avoidance concerns. Cows that had at least one quarter that yielded 
1 cfu per 0.01 ml of milk of S. aureus on either of these first two samples, were defined as infected. These cows were sampled for a third time at drying-off (d 0) and randomly assigned to receive, in all four quarters, either intramammary benzathine cloxacillin (Dry Clox, Ayerst Laboratory, Guelph, Ontario) or a novel intramammary formulation of tilmicosin phosphate (supplied by Provel, Division of Eli Lilly Canada Inc., Guelph, Ontario, Canada). The intramammary infusion of DCT was done by the technician as soon as possible after the last milking, and was administered by the partial insertion technique. Following the subsequent calving, all cows were sampled three times during the first month of lactation at 3 to 9, 10 to 16, and 24 to 30 DIM. Quarters that were infected before the dry period were considered to be cured if they were culture negative for S. aureus on all three samples taken in the first month of lactation. A cow was defined as cured if all infected quarters before drying-off were culture negative on all three samples after freshening.
Herd Management and Other Data Collection
During one of the scheduled visits to each farm, the technician at each site administered a comprehensive herd survey. Data collected included housing style, milking hygiene practices, management of the environment for both lactating and dry cows, as well as routine drying-off procedures used by each individual farm. Management factors used to determine appropriate drying-off time, and specific practices such as abrupt versus intermittent cessation of milking, gram-negative core-antigen vaccination, and teat-end protection were collected. Individual cow DHI data for the last three DHI tests before and including the month of drying-off, were collected. The data consisted of dry period length, SCC, linear score (LS), 305 mature equivalent milk, and 24-h yields of milk, fat and protein.
Bacteriological Procedures
Teats were aseptically prepared before collection of all samples according to National Mastitis Council sample collection and handling guidelines (NMC, 1999). Samples were frozen and shipped to the Mastitis Research Laboratory at the University of Guelph. All laboratory procedures were performed by the same individuals, who were blinded to treatment, and in accordance with NMC recommendations (NMC, 1999). Briefly, depending on the day of arrival at the lab, samples were either thawed at room temperature or stored at -20°C for a period of not longer than 5 d, and then thawed the first day of the following week. An inoculum of 0.01 ml of milk was plated onto Columbia base agar containing 5% sheep blood. Plates were incubated at 37°C and examined for bacterial growth at 24 and 48 h. Colonies were tentatively identified, and a presumptive diagnosis of staphylococci, streptococci, coliform, or other pathogens was made, based on colony growth, morphology and appearance, pattern of hemolysis, catalase reaction, and Gram staining. Staphylococcal isolates were tested for coagulase production with the tube coagulase test. Streptococcal isolates were further subcultured with agar containing esculin. Gram-negative bacteria were plated on MacConkey agar to facilitate identification. Gross appearance and reaction to citrate were used to differentiate Escherichia coli and Klebsiella spp. For each positive quarter, the number of cfu per 0.01 ml of milk was reported in one of four categories: 1 to 5, 6 to 10, 11 to 50 or 50 cfu. A quarter was considered infected with coagulase-negative staphylococci (CNS) if greater than or equal to 11 cfu per 0.01 ml were isolated. The isolation of CNS was reported when the organism grew with another pathogen. A sample was considered contaminated if three or more colony types were present on a plate. Since all samples were frozen, quarter SCC determination was not performed.
Statistical Analysis
Data generated from the quarter milk cultures, herd management surveys and individual cow DHI records, were stored in a Microsoft Access database (Microsoft Access 2000). Only those herds that participated in the trial for its entire length, and that had S. aureus isolated from at least one cow during that time, provided the data analyzed in this study. Records for 308 quarters infected with S. aureus from 219 cows on 59 farms were extracted from the database and imported into SAS version 8.01 (SAS, 1999). There were 18 farms in which cows infected with S. aureus were either not identified, or cows were identified but they did not complete the trial. Descriptive statistics were generated using the univariate and frequency procedure in SAS (PROC UNIVARIATE, PROC FREQ, SAS v.8.01). Differences in cure rates were tested with a chi-square (
2) analysis. Least square means for linear scores (LS) at drying-off were calculated (PROC GLM) and differences examined using a Student’s t-test. Logistic regresion for cure or no cure of S. aureus infection was modeled by fitting a generalized linear model using the GENMOD procedure, with the logit link function, and a binomial error distribution. Because quarters within a cow are not independent, correlation within cows was accounted for using generalized estimation equations (Liang and Zeger, 1986; Barkema, 1997). A compound symmetry correlation structure was used. Data were analyzed by quarter, cow, and herd levels, acknowledging that there was clustering of quarters within a cow, as well as of cows within a herd. The variance components at both the herd and cow level were evaluated to decide whether cow and herd effects would be considered as either random or fixed effects in the final model. Since herds had a very low variance component, the most appropriate and best fitting model included herd as a fixed effect and cows within herds as a clustering variable. In fitting herds as a fixed effect, a herd size variable was created to identify each herd that had more than 100 cows. This allowed comparison between these herds, as well as to those that were smaller in size. This distinction was necessary, as the model did not converge when a parameter was estimated for each individual herd. The choice of herd size was based on inherent differences in management strategies and housing styles associated with larger herds.
A variable to quantify the degree of shedding was created using the reported colony-forming units on each positive sample. The original results from the laboratory were reported in categories, thus the variable created was categorical. A bacteriology result of 1 to 5 cfu was given a code of 1, 6–10 cfu a code of 2, 11–50 cfu coded 3, and greater than 50 cfu coded 4. Hence, if a cow had three positive samples that were coded 3, 3, and 4, the shedding code assigned to that cow was 10. To assess the effect that the month of drying-off had on the cure rate, a season variable was created using 3-mo intervals. Spring was designated as March-May, Summer as June-August, Fall as September-November, and winter included December to February. A univariate model with each independent variable of interest was evaluated first, with all significant variables at P < 0.20 allowed to enter the multivariable model. Relaxing the P value for entry into the model was used as a method to ensure all covariates, with a potential to exert significant main effects as well as important confounding effects, were considered. A backwards step-wise procedure was used to determine the final model. Statistical significance was declared at P < 0.05, but variables with P < 0.10 were allowed to stay in the model based on a tendency towards significance, and if these associations were deemed to be of biological importance. All biologically plausible two-way interactions were tested. The estimated regression parameters were converted to odds ratios.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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and 2. Of the 219 S. aureus positive cows, 154 (70.3%) had only one quarter infected. The percentage with two, three, or four infected quarters were 21.5, 5.5, and 2.7%, respectively. The average LS as reported on the last DHI test in the month of drying-off was 5.3. There was a significant difference in the mean LS of cows based on the number of quarters infected (Table 1). A calcualtion of the mean prevalence of S. aureus within herds was made, by using the number of cows identified as infected in a herd divided by the total herd size. The mean was found to be 7% in the 59 herds with a range of 1.2 to 36%.
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). The cure rate for quarters that cultured positive on one sample was significantly higher than quarters that cultured positive multiple times. The distribution of the location of the infected quarters was approximately equal between front and hind quarters (47 and 53%, respectively).
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). By comparison, the cure achieved with intramammary cloxacillin was 56.9% of cows and 62.9% of quarters. The results of unconditional univariate analysis determined that this difference in cure rates between treatments was not statistically significant at the P < 0.05 level for either cow or quarter cure rates (Table 2).
Cure rates were seen to be higher in cows that were finishing their first lactation, that had a LS of less than 5 on their last DHI test. There was a statistically significant difference in the cure rate based on LS on last DHI test: 70.9% of cows cured that were at LS < 5, compared with 56.4% that were at LS 5 (P < 0.05). The highest cure rate was observed in cows that had three quarters infected (83.3%). The percentage of cows that cured with one, two, or four quarters infected were 65.6, 46.8, and 50%, respectively (Table 2).
Logistic Regression Analysis
Quarter level.
The logistic regression model for cure of quarters is shown in Table 3. Variables predicting the probability of bacteriologic cure in an infected quarter included the number of samples that cultured positive, location of the quarter and the use of tilmicosin DCT (Table 2). The fixed effect herd size variable was forced into the final model. When accounting for the other variables in the model, the use of tilmicosin DCT resulted in a higher probability for cure of S. aureus (P = 0.04). The odds ratio (OR) for cure comparing tilmicosin DCT to cloxacillin was 1.8. The probability of cure increased when the infection was in a front quarter (OR = 2.3). There was a decreased risk of cure with an increasing number of positive samples before drying-off (OR = 0.6). A higher LS, based on DHI testing at the cow level, tended to decrease the probability of cure at the quarter level (P = 0.08). LS was a significant risk factor for cow level cure (P = 0.05). The presence of a CNS infection in the same quarter infected with S. aureus was associated with a much higher OR for cure (5.1). The effect was nonsignificant but may be biologically important due to its magnitude. The goodness of fit of the model was assessed by the departure of the model deviance from the degrees of freedom. The deviance of this final model is 308 with 289 df, which indicated acceptable fit.
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. Risk factors for bacteriological cure of cows included LS on the last DHI test, bacterial shedding, season of drying-off, as well as intramammary treatment with tilmicosin. At the cow level, intramammary tilmicosin remained a significant factor in the model (P = 0.03). A cow treated with tilmicosin has a 2.1 times greater chance of curing S. aureus, compared with a cow treated with cloxacillin. The variable ‘shedding’ was significant (P = 0.0002), indicating that as the degree of S. aureus shed increased, the probability of cure decreased. Clearly, an equivalent shedding variable could be generated from large numbers of bacteria shed from one quarter or from moderate numbers shed from multiple quarters. Therefore, the interaction of shedding and number of infected quarters was tested and found to be significant (P = 0.002). This interaction indicated that lower shedding per infected quarter had a somewhat better probability of cure. There was a significant effect, at the cow level, for season to impact the probability of cure. In comparison to cows that were dried off in the spring season (March-May), cows that were dried off during the winter (December-February) were 4 times more likely to cure S. aureus infection (P = 0.004). Age of the cow and dry period length were not significant risk factors for S. aureus cure either at the quarter or cow level. With 198 df and a deviance of 221, the fit of the model was acceptable.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Benzathine cloxacillin was used as the positive control in this field trial, as it has been commercially available and used for approximately 20 yr (Keefe, 1980). Cloxacillin is a semisynthetic penicillin. When it was first evaluated as a DCT, the rates of elimination of S. aureus when administered at drying-off were 85 and 77% in controlled and field trial experiments, respectively. One year later, Ziv et al. (1981) published efficacy data comparing three antibiotics at drying-off, one of which was a derivative of benzathine cloxacillin. This data revealed a mean cure rate of S. aureus from all three treatments during the dry period of 81.4%. The cure rate for benzathine cloxacillin was 83.1%.
The most recently published efficacy data for the use of tilmicosin at drying-off was reported by Nickerson et al. (1999), who used cephapirin benzathine as a positive control. This study demonstrated that an experimental intramammary formulation of tilmicosin was equally as effective as cephapirin benzathine for eliminating S. aureus mastitis at both the cow and quarter levels, with tilmicosin achieving 64.3 and 78.1% cure rates, respectively. The main difference between Nickerson’s study and the current field trial, other than the positive control used, was the nature of the infections. The previously cited numbers were obtained following dry cow therapy of 44 cows, the majority of which had infections that were experimentally induced. The cure rates for both intramammary treatments were consistently higher for experimental infections than those caused naturally (Nickerson et al., 1999). The current study was done in commercial and research farms in three geographical regions of Canada, with cows that were naturally infected, and identified through the culture of quarter milk samples collected prior to drying-off.
An important consideration that must be addressed whenever efficacy data for therapy of mastitis pathogens, especially for cure rates of S. aureus, are reported, are the definitions of infection and treatment cure. In this current study, the definition of infection before drying-off was at least one of three samples being culture positive (1 cfu/0.01 ml) for S. aureus. Based on the fact that approximately 80% of the infections in this trial actually cultured positive on multiple samples before drying-off, confidence that these quarters and cows were indeed infected with S. aureus seems reasonable. Furthermore, these animals were probably a good representation of naturally infected cows in commercial herds. However, there were 20.1% of quarters in this dataset that had only a single isolation of S. aureus, and there was also an underlying assumption that when S. aureus was not isolated, that an infection did not exist. Intermittent and cyclical shedding of S. aureus does occur (Sears et al., 1990). Sears et al. (1990) studied the shedding patterns of S. aureus and the implication of shedding patterns when evaluating the efficacy of antimicrobial drugs. They concluded that the cyclical pattern of shedding necessitates consecutive samples. The probability of at least one sample being positive from a S. aureus-infected quarter when three samples are taken was estimated at 98% (Sears et al., 1990). Based on this fact, both the definition of infection and the definition of cure in this trial were made on three consecutive samples. The decision to extend the sampling out of 30 DIM in the subsquent lactation was deemed appropriate, by earlier research which established that it may take up to 28 d for a S. aureus infection to reappear (Newbould, 1974). Another more recently identified aspect of S. aureus cure and sampling, is the identification of the particular strain of S. aureus through DNA technologies (Zadoks, 2000). This technology was not incorporated into this research trial. Thus, there is a possibility that some treatment failures in efficacy trials, such as the current study, may indeed be misclassified and are actually a combination of a cure and a new infection caused by an entirely different strain of the same organism (Schukken et al., 2001).
Regardless of the efficacy of any one treatment regime of therapeutic approach, emphasis should be placed on identifying cows that have a high probability of cure. Because antibiotic use on dairy farms is under increasing scrutiny, considering opportunties for more rational and selective use of DCT is of value (Schukken et al., 2001). The results of this study indicate that risk factors for cure of quarters infected with S. aureus are the number of positive cultures, the location of the quarter, and possibly a coexisting CNS infection (P < 0.10). S. aureus IMI was less likely to be cured in quarters that were culture positive more than once. Also, cure of S. aureus was less likely to occur when the infection was in a rear quarter. These risk factors have been previously reported (Sol et al., 1994; Osteras et al., 1999). Indeed, there is a possibility that the number of positive samples may be a surrogate measure of severity or chronicity. Also there is a possibility that only a single isolation of S. aureus may not truly have been an infection. The repeatability of the significance of the location of the quarter is surprising. Osteras et al. (1999) established even more specifically the predictive failure of an infection with a major pathogen in the right hind quarter, not just a hind quarter. The authors hypothesized in that study that more persistent infections in the right hind quarter might result from hygienic contamination caused by laterality or side-specific interference of blood circulation. No information was gathered in this study to refute or support this claim, or to offer any other hypothesis either. The repeatability of this finding however, should be the attention of further work.
The linear score of the cow in the month before drying-off had a tendency to significantly impact the quarter level cure rate (P = 0.08). As the linear score increased, the probability for cure of an infected quarter decreased (OR = 0.8). There was no expectation that a cow level measure such as LS would have that strong of an influence at the quarter level. However, this is likely because 70% of infected cows in this trial only had one quarter infected with S. aureus. Similar to the number of positive samples, a high LS is probably indicative of a more severe infection. Sol et al. (1994), also found that an increasing SCC decreased the probability of quarter cure. The other biologically significant finding at the quarter level was the tendency for an existing infection caused by CNS to increase the probability of cure (P = 0.08). This finding is based on only a very small number of quarters that had both CNS and S. aureus isolated. The literature indicates that minor pathogen infections have a protective effect against the establishment of S. aureus infections (Nickerson et al., 1994; Lam et al., 1997; Schukken et al., 1999). Because these infections were identified at the same time as the S. aureus, this may not be a readily plausible explanation for the effect seen here. Competition between the two organisms has been described and can result in a shorter duration of S. aureus infection (Lam et al., 1997). However, the mechanism producing the protection effect is not fully understood. General activation of the immune system, competition for binding sites and alterations in teat canal keratin are offered as possible explanations (Rainard et al., 1988; Nickerson et al., 1994; Lam et al., 1997).
Risk factors for cure of cows infected with S. aureus included LS on the last DHI test before drying-off and the amount of bacteria being shed by the cow. As LS and the amount of bacteria shed increase, the likelihood of a cure diminished. The other factor found to be significantly associated with the cure rate of S. aureus-infected cows in this research was the season of drying-off. Cows dried off from December to February had a significantly higher cure rate. Biologically satisfying reasons for this effect are not apparent. There was not a significant association with the number of quarters positive for S. aureus, as a determinant on its own. However, there was an interaction between the number of quarters and shedding, and as reported in Table 2, the highest proportion of cure was observed in the 12 cows that had three quarters infected (83.3%). However, Sol et al. (1994) reported that cows with more than one quarter infected were 0.57 times less likely to cure. Our result is similar to the finding of Nickerson et al. (1999), who also reported that cure rates for intramammary tilmicosin were not influenced by either the number of quarters infected or by the lactation number. There was also no association between the probability of cure and dry period length. A positive correlation between a SCC measure and dry period length can reduce the effect of both variables individually (Sol et al., 1994). LS on the last DHI test was significant in the model for cure at the cow level. Thus, the finding that dry period was not a risk factor may be reasonable since these two variables were moderately correlated in this data (r = 0.56).
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Received for publication January 5, 2002. Accepted for publication April 9, 2002.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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i
, J. A. C. M. Lohuis, J. A. M. de Hoog, and B. Poutrel. 2000. Location of Staphylococcus aureus within the experimentally infected bovine udder and the expression of capsular polysaccharide type 5 in situ. J. Dairy Sci. 83:1966–1975.[Abstract]
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