Antibiotic Resistance of Staphylococci from Bulk-Tank Milk of Sheep Flocks: Prevalence, Patterns, Association with Biofilm Formation, Effects on Milk Quality, and Risk Factors
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sheep Flocks and Sampling
2.2. Laboratory Examinations
2.3. Data Management and Analysis
2.3.1. Data Management
2.3.2. Statistical Analysis
3. Results
3.1. Staphylococcal Recovery and Presence of Antibiotic Resistance
3.2. Biofilm Formation
3.3. Associations with Milk Quality
3.4. Variables Associated with Isolation of Resistant Staphylococcal Isolates from the Bulk-Tank Milk
3.4.1. Isolation of Oxacillin-Resistant Staphylococcal Isolates
3.4.2. Isolation of Staphylococcal Isolates Resistant to at Least One Antibiotic
3.4.3. Isolation of Multi-Resistant Staphylococcal Isolates
4. Discussion
4.1. Presence of Antibiotic Resistance in Staphylococcal Isolates
4.2. Association of Antibiotic Resistance with Biofilm Formation
4.3. Possible Effects on Milk Quality
4.4. Predictors for Antibiotic-Resistant Staphylococcal Isolates
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Management system applied in the flock (description according to EFSA classification) [47] |
Month into the lactation period at sampling (month) |
Machine- or hand-milking (description) |
No. of ewes in the flock (no.) |
Total milk quantity per ewe obtained during the preceding milking period (litres) |
Average number of lambs born per ewe (no.) |
Collaboration with a veterinarian (yes/no) |
Total visits made annually by veterinarians to the flock during the preceding season (no.) |
Clinical mastitis annual incidence risk in the flock (%) |
Age of lamb removal from their dams (days) |
Daily number of milking sessions (no.) |
Duration of the dry-period (months) |
Means of calculating live bodyweight for the administration of pharmaceutical products (weighing/estimation) |
Routine overdosing (compared to dose prescribed) of pharmaceuticals (yes/no) |
Annual frequency of systemic disinfections in the farm (no. of occasions) |
Routine administration of antimicrobials in newborns (yes/no) |
Vaccination against mastitis (yes/no) |
Administration of ‘dry-ewe’ treatment at the end of the lactation period (yes/no) |
Use of teat disinfection after milking (yes/no) |
Age of the farmer (years) |
Length of previous animal farming experience of the farmer (years) |
Education of the farmer (description) |
Farmer by profession (yes/no) |
Family tradition in farming (yes/no) |
Presence of working staff in the flock (yes/no) |
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Staphylococcal Species | Frequency of Staphylococcal Isolates | ||
---|---|---|---|
All Isolates 1 | Resistant Isolates 2,3 | Multi-Resistant Isolates 3,4 | |
Staphylococcus aureus | 54 (0.233) | 17 (0.315) | 2 (0.037) |
Staphylococcus simulans | 35 (0.151) | 4 (0.114) | 0 (0.000) |
Staphylococcus equorum | 23 (0.099) | 17 (0.739) | 14 (0.609) |
Staphylcoccus haemolyticus | 22 (0.095) | 11 (0.500) | 1 (0.045) |
Staphylococcus chromogenes | 13 (0.056) | 4 (0.308) | 1 (0.077) |
Staphylococcus lentus | 12 (0.051) | 11 (0.917) | 8 (0.667) |
Staphylococcus lugdunensis | 11 (0.047) | 7 (0.636) | 1 (0.091) |
Staphylococcus warneri | 9 (0.039) | 3 (0.333) | 1 (0.111) |
Staphylococcus kloosii | 7 (0.030) | 5 (0.714) | 4 (0.571) |
Staphylococcus capitis | 6 (0.026) | 3 (0.500 | 0 (0.000) |
Staphylococcus intermedius | 6 (0.026) | 3 (0.500) | 0 (0.000) |
Staphylococcus cohnii subsp. cohnii | 4 (0.017) | 3 (0.750) | 1 (0.250) |
Staphylococcus epidermidis | 4 (0.017) | 4 (1.000) | 0 (0.000) |
Staphylococcus saprophyticus | 4 (0.017) | 2 (0.500) | 2 (0.500) |
Staphylococcus xylosus | 4 (0.017) | 3 (0.750) | 3 (0.750) |
Staphylococcus auricularis | 3 (0.013) | 2 (0.667) | 0 (0.000) |
Staphylococcus cohnii subsp. urealyticum | 3 (0.013) | 2 (0.667) | 1 (0.333) |
Staphylococcus sciuri | 3 (0.013) | 1 (0.333) | 1 (0.333) |
Staphylococcus vitulinus | 3 (0.013) | 1 (0.333) | 1 (0.333) |
Staphylococcus hominis | 2 (0.009) | 1 (0.500) | 0 (0.000) |
Staphylococcus pasteuri | 2 (0.009) | 2 (1.000) | 0 (0.000) |
Staphylococcus carnosus | 2 (0.009) | 1 (0.500) | 0 (0.000) |
Total | 232 (1.000) | 107 (0.461) | 41 (0.177) |
Variable (n = 1) | Odds Ratio 1 (95% Confidence Intervals) | p |
---|---|---|
Length of previous animal farming experience of farmers | 0.018 | |
≤5 years (n = 74) | 2.747 (1.202–6.276) | 0.017 |
>5 years (n = 251) | Reference |
Variable (n = 1) | Odds Ratios 1 (95% Confidence Intervals) | p |
---|---|---|
Month into the lactation period at sampling | 0.003 | |
0th to 1st (n = 23) | 6.067 (1.361–27.050) | 0.018 |
2nd to 5th (n = 138) | 2.258 (0.617–8.259) | 0.218 |
6th to 9th (n = 147) | 1.627 (0.443–5.973) | 0.463 |
Subsequently to 9th (n = 17) | Reference |
Variable (n = 1) | Odds Ratios 1 (95% Confidence Intervals) | p |
---|---|---|
Management system applied in the flock | 0.015 | |
Intensive (n = 43) | 13.939 (1.745–111.329) | 0.013 |
Semi-intensive (n = 151) | 3.512 (0.449–27.460) | 0.23 |
Semi-extensive (n = 107) | 1.859 (0.221–15.606) | 0.57 |
Extensive (n = 24) | Reference |
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Lianou, D.T.; Petinaki, E.; Cripps, P.J.; Gougoulis, D.A.; Michael, C.K.; Tsilipounidaki, K.; Skoulakis, A.; Katsafadou, A.I.; Vasileiou, N.G.C.; Giannoulis, T.; et al. Antibiotic Resistance of Staphylococci from Bulk-Tank Milk of Sheep Flocks: Prevalence, Patterns, Association with Biofilm Formation, Effects on Milk Quality, and Risk Factors. Biology 2021, 10, 1016. https://doi.org/10.3390/biology10101016
Lianou DT, Petinaki E, Cripps PJ, Gougoulis DA, Michael CK, Tsilipounidaki K, Skoulakis A, Katsafadou AI, Vasileiou NGC, Giannoulis T, et al. Antibiotic Resistance of Staphylococci from Bulk-Tank Milk of Sheep Flocks: Prevalence, Patterns, Association with Biofilm Formation, Effects on Milk Quality, and Risk Factors. Biology. 2021; 10(10):1016. https://doi.org/10.3390/biology10101016
Chicago/Turabian StyleLianou, Daphne T., Efthymia Petinaki, Peter J. Cripps, Dimitris A. Gougoulis, Charalambia K. Michael, Katerina Tsilipounidaki, Anargyros Skoulakis, Angeliki I. Katsafadou, Natalia G. C. Vasileiou, Themis Giannoulis, and et al. 2021. "Antibiotic Resistance of Staphylococci from Bulk-Tank Milk of Sheep Flocks: Prevalence, Patterns, Association with Biofilm Formation, Effects on Milk Quality, and Risk Factors" Biology 10, no. 10: 1016. https://doi.org/10.3390/biology10101016