Bovine subclinical mastitis-associated methicillin-resistant Staphylococcus aureus, selective genotyping and antimicrobial susceptibility profile of the isolates in Kurdistan province of Iran
Abstract
Background and Objectives: Staphylococcus aureus is frequently involved in bovine subclinical mastitis worldwide. Besides, the methicillin-resistant S. aureus (MRSA) carrier state of animals is a matter of worrisome. This study aimed to evaluate the frequency of MRSA, discriminatory geno-analysis and antibiotic resistance scheme of the strains isolated from bovine subclinical mastitis in Kurdistan province of Iran.
Materials and Methods: A total of 283 samples were collected and analyzed for S. aureus phenotypically and molecularly. SCCmec and coa types, and pvl gene were evaluated using polymerase chain reaction (PCR). Finally, the restriction fragment length polymorphism (RFLP) patterns of coa types and the antimicrobial susceptibility profile of the isolates were assessed.
Results: Among the 95 isolates of S. aureus, 11 (11.57%) strains were recognized as MRSA. Six, one, and four SCCmec types represented for IVa, IVc, and V were determined, respectively, among which an individual IVa and V determinant harboured pvl gene. Restriction digestion products of 490 bp, 680 bp, and 730 bp of coa bands were generated. Tobramycin, mupirocin, fusidic acid, clindamycin, and chloramphenicol were the most effective drugs against the MRSA isolates.
Conclusion: The detrimental involvement of S. aureus in bovine subclinical mastitis is proved herein. Besides, the contribution of MRSA and potential contamination of milk and dairy products with the bacterium may impose a serious public health risk. This demands serious and long-lasting efforts to control the infection. The results may be effective in the implementation of accurate controlling strategies.
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2. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 2007;13:222-235.
3. Ahangari Z, Ghorbanpoor M, Seifiabad Shapouri MR, Gharibi D, Ghazvini K. Methicillin resistance and selective genetic determinants of Staphylococcus aureus isolates with bovine mastitis milk origin. Iran J Microbiol 2017;9:152-159.
4. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 2003;111:1265-1273.
5. Wu Z, Li F, Liu D, Xue H, Zhaoa X. Novel type XII Staphylococcal cassette chromosome mec harboring a new cassette chromosome recombinase, CcrC2. Antimicrob Agents Chemother 2015;59:7597-7601.
6. Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 2007;87:3-9.
7. Kaida S, Miyata T, Yoshizawa Y, Kawabata S, Morita T, Igarashi H, et al. Nucleotide sequence of the staphylocoagulase gene: its unique COOH-terminal 8 tandem repeats. J Biochem 1987;102:1177-1186.
8. Dastmalchi Saei H, Ahmadi M, Mardani K, Batavani RA. Molecular typing of Staphylococcus aureus isolated from bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Vet Microbiol 2009;137:202-206.
9. Momtaz H, Tajbakhsh E, Rahimi E, Momeni M. Coagulase gene polymorphism of Staphylococcus aureus isolated from clinical and sub-clinical mastitis in Isfahan and Chaharmahal va Bakhtiari provinces of Iran. Comp Clin Path 2011;20:519-522.
10. Dastmalchi Saei H. coa types and antimicrobial resistance profile of Staphylococcus aureus isolates from cases of bovine mastitis. Comp Clin Path 2012;21:301-307.
11. Haran KP, Godden SM, Boxrud D, Jawahir S, Bender JB, Sreevatsan S. Prevalence and characterization of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. J Clin Microbiol 2012;50:688-695.
12. Schalm O, Noorlander D. Experiments and observations leading to the development of California mastitis test. J Am Vet Med Assoc 1957;130:199-204.
13. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992;30:1654-1660.
14. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: Twenty-ninth Informational Supplement: Document M100. Wayne, PA, USA: CLSI 2019.
15. Geha DJ, Uhl JR, Gustaferro CA, Persing DH. Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 1994;32:1768-1772.
16. Ghaznavi-Rad E, Nor Shamsudin M, Sekawi Z, van Belkum A, Neela V. A simplified multiplex PCR assay for fast and easy discrimination of globally distributed staphylococcal cassette chromosome mec types in methicillin resistant Staphylococcus aureus. J Med Microbiol 2010;59:1135-1139.
17. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999;29:1128-1132.
18. Hookey JV, Richardson JF, Cookson BD. Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. J Clin Microbiol 1998;36:1083-1089.
19. Gindonis V, Taponen S, Myllyniemi AL, Pyörälä S, Nykäsenoja S, Salmenlinna S, et al. Occurrence and characterization of methicillin-resistant staphylococci from bovine mastitis milk samples in Finland. Acta Vet Scand 2013;55:61.
20. Havaei SA, Assadbeigi B, Esfahani BN, Hoseini NS, Rezaei N, Havaei SR. Detection of mecA and enterotoxin genes in Staphylococcus aureus isolates associated with bovine mastitis and characterization of Staphylococcal cassette chromosome mec (SCCmec) in MRSA strains. Iran J Microbiol 2015;7:161-167.
21. Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Vet Microbiol 2010;144:166-171.
22. Bardiau M, Yamazaki K, Duprez JN, Taminiau1 B, Mainil JG, Ote I. Genotypic and phenotypic characterization of methicillin resistant Staphylococcus aureus (MRSA) isolated from milk of bovine mastitis. Lett Appl Microbiol 2013;57:181-186.
23. Hata E. Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus New York/Japan clone. J Vet Diagn Invest 2016;28:291-298.
24. Kumar R, Yadav BR, Singh RS. Antibiotic resistance and pathogenicity factors in Staphylococcus aureus isolated from mastitic Sahiwal cattle. J Biosci 2011;36:175-188.
25. Hoquea MN, Dasa ZC, Rahmana ANMA, Haiderb MG, Islamc MA. Molecular characterization of Staphylococcus aureus strains in bovine mastitis milk in Bangladesh. Int J Vet Sci Med 2018;6:53-60.
26. Pumipuntu N, Tunyong W, Chantratita N, Diraphat P, Pumirat P, Sookrung N, et al. Staphylococcus spp. associated with subclinical bovine mastitis in central and northeast provinces of Thailand. PeerJ 2019;7:e6587.
27. Ahmadi E, Djeddi AN, Mousavi SA. Prevalence of coagulase negative staphylococcus including methicillin resistant strains in buffalo subclinical mastitis in Northwest of Iran. Buffalo Bull 2020;39:17-26.
28. Ahmadi E, Khojasteh M, Mortazavi SM, Khan-Mohammadi F, Kazemnia A, Beheshtipour J, et al. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus nasal carriage in the West of Iran: a population-based cross-sectional study. BMC Infect Dis 2019;19:899.
29. da Silva ER, da Silva N. Coagulase gene typing of Staphylococcus aureus isolated from cows with mastitis
in southeastern Brazil. Can J Vet Res 2005;69:260-264.
30. Goh SH, Byrne SK, Zhang JL, Chow AW. Molecular typing of Staphylococcus aureus on the basis of coagulase gene polymorphisms. J Clin Microbiol 1992;30:1642-1645.
31. Moon JS, Lee AR, Kang HM, Lee ES, Joo YS, Park YH, et al. Antibiogram and coagulase diversity in staphylococcal enterotoxin-producing Staphylococcus aureus from bovine mastitis. J Dairy Sci 2007;90:1716-1724.
32. Gentilini E, Denamiel G, Llorente P, Godaly S, Rebuelto M, DeGregorio O. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Argentina. J Dairy Sci 2000;83:1224-1227.
33. Ebrahimi A, Akhavan Taheri M. Characteristics of staphylococci isolated from clinical and subclinical mastitis cows in Shahrekord-Iran. Iran J Vet Res 2009;10:273-277.
34. Gandhale D, Kolhe R, Nalband SD, Jagtap U, Dhandore C, Bhave S, et al. Molecular types and antimicrobial resistance profile of Staphylococcus aureus isolated from dairy cows and farm environments. Turkish J Vet Anim Sci 2017;41:713-724.
35. Feng Y, Qi W, Xu-rong W, Ling W, Xin-pu L, Jin-yin L, et al. Genetic characterization of antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis cases in Northwest China. J Integr Agric 2016;15:2842-2847.
2. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 2007;13:222-235.
3. Ahangari Z, Ghorbanpoor M, Seifiabad Shapouri MR, Gharibi D, Ghazvini K. Methicillin resistance and selective genetic determinants of Staphylococcus aureus isolates with bovine mastitis milk origin. Iran J Microbiol 2017;9:152-159.
4. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 2003;111:1265-1273.
5. Wu Z, Li F, Liu D, Xue H, Zhaoa X. Novel type XII Staphylococcal cassette chromosome mec harboring a new cassette chromosome recombinase, CcrC2. Antimicrob Agents Chemother 2015;59:7597-7601.
6. Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 2007;87:3-9.
7. Kaida S, Miyata T, Yoshizawa Y, Kawabata S, Morita T, Igarashi H, et al. Nucleotide sequence of the staphylocoagulase gene: its unique COOH-terminal 8 tandem repeats. J Biochem 1987;102:1177-1186.
8. Dastmalchi Saei H, Ahmadi M, Mardani K, Batavani RA. Molecular typing of Staphylococcus aureus isolated from bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Vet Microbiol 2009;137:202-206.
9. Momtaz H, Tajbakhsh E, Rahimi E, Momeni M. Coagulase gene polymorphism of Staphylococcus aureus isolated from clinical and sub-clinical mastitis in Isfahan and Chaharmahal va Bakhtiari provinces of Iran. Comp Clin Path 2011;20:519-522.
10. Dastmalchi Saei H. coa types and antimicrobial resistance profile of Staphylococcus aureus isolates from cases of bovine mastitis. Comp Clin Path 2012;21:301-307.
11. Haran KP, Godden SM, Boxrud D, Jawahir S, Bender JB, Sreevatsan S. Prevalence and characterization of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. J Clin Microbiol 2012;50:688-695.
12. Schalm O, Noorlander D. Experiments and observations leading to the development of California mastitis test. J Am Vet Med Assoc 1957;130:199-204.
13. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992;30:1654-1660.
14. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: Twenty-ninth Informational Supplement: Document M100. Wayne, PA, USA: CLSI 2019.
15. Geha DJ, Uhl JR, Gustaferro CA, Persing DH. Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 1994;32:1768-1772.
16. Ghaznavi-Rad E, Nor Shamsudin M, Sekawi Z, van Belkum A, Neela V. A simplified multiplex PCR assay for fast and easy discrimination of globally distributed staphylococcal cassette chromosome mec types in methicillin resistant Staphylococcus aureus. J Med Microbiol 2010;59:1135-1139.
17. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999;29:1128-1132.
18. Hookey JV, Richardson JF, Cookson BD. Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. J Clin Microbiol 1998;36:1083-1089.
19. Gindonis V, Taponen S, Myllyniemi AL, Pyörälä S, Nykäsenoja S, Salmenlinna S, et al. Occurrence and characterization of methicillin-resistant staphylococci from bovine mastitis milk samples in Finland. Acta Vet Scand 2013;55:61.
20. Havaei SA, Assadbeigi B, Esfahani BN, Hoseini NS, Rezaei N, Havaei SR. Detection of mecA and enterotoxin genes in Staphylococcus aureus isolates associated with bovine mastitis and characterization of Staphylococcal cassette chromosome mec (SCCmec) in MRSA strains. Iran J Microbiol 2015;7:161-167.
21. Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Vet Microbiol 2010;144:166-171.
22. Bardiau M, Yamazaki K, Duprez JN, Taminiau1 B, Mainil JG, Ote I. Genotypic and phenotypic characterization of methicillin resistant Staphylococcus aureus (MRSA) isolated from milk of bovine mastitis. Lett Appl Microbiol 2013;57:181-186.
23. Hata E. Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus New York/Japan clone. J Vet Diagn Invest 2016;28:291-298.
24. Kumar R, Yadav BR, Singh RS. Antibiotic resistance and pathogenicity factors in Staphylococcus aureus isolated from mastitic Sahiwal cattle. J Biosci 2011;36:175-188.
25. Hoquea MN, Dasa ZC, Rahmana ANMA, Haiderb MG, Islamc MA. Molecular characterization of Staphylococcus aureus strains in bovine mastitis milk in Bangladesh. Int J Vet Sci Med 2018;6:53-60.
26. Pumipuntu N, Tunyong W, Chantratita N, Diraphat P, Pumirat P, Sookrung N, et al. Staphylococcus spp. associated with subclinical bovine mastitis in central and northeast provinces of Thailand. PeerJ 2019;7:e6587.
27. Ahmadi E, Djeddi AN, Mousavi SA. Prevalence of coagulase negative staphylococcus including methicillin resistant strains in buffalo subclinical mastitis in Northwest of Iran. Buffalo Bull 2020;39:17-26.
28. Ahmadi E, Khojasteh M, Mortazavi SM, Khan-Mohammadi F, Kazemnia A, Beheshtipour J, et al. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus nasal carriage in the West of Iran: a population-based cross-sectional study. BMC Infect Dis 2019;19:899.
29. da Silva ER, da Silva N. Coagulase gene typing of Staphylococcus aureus isolated from cows with mastitis
in southeastern Brazil. Can J Vet Res 2005;69:260-264.
30. Goh SH, Byrne SK, Zhang JL, Chow AW. Molecular typing of Staphylococcus aureus on the basis of coagulase gene polymorphisms. J Clin Microbiol 1992;30:1642-1645.
31. Moon JS, Lee AR, Kang HM, Lee ES, Joo YS, Park YH, et al. Antibiogram and coagulase diversity in staphylococcal enterotoxin-producing Staphylococcus aureus from bovine mastitis. J Dairy Sci 2007;90:1716-1724.
32. Gentilini E, Denamiel G, Llorente P, Godaly S, Rebuelto M, DeGregorio O. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Argentina. J Dairy Sci 2000;83:1224-1227.
33. Ebrahimi A, Akhavan Taheri M. Characteristics of staphylococci isolated from clinical and subclinical mastitis cows in Shahrekord-Iran. Iran J Vet Res 2009;10:273-277.
34. Gandhale D, Kolhe R, Nalband SD, Jagtap U, Dhandore C, Bhave S, et al. Molecular types and antimicrobial resistance profile of Staphylococcus aureus isolated from dairy cows and farm environments. Turkish J Vet Anim Sci 2017;41:713-724.
35. Feng Y, Qi W, Xu-rong W, Ling W, Xin-pu L, Jin-yin L, et al. Genetic characterization of antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis cases in Northwest China. J Integr Agric 2016;15:2842-2847.
| Files | ||
| Issue | Vol 13 No 1 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i1.5494 | |
| Keywords | ||
| Mastitis; Bovine; Methicillin-resistant Staphylococcus aureus; Genetic profile; Antibacterial drugs resistance | ||
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How to Cite
1.
Khazaie F, Ahmadi E. Bovine subclinical mastitis-associated methicillin-resistant Staphylococcus aureus, selective genotyping and antimicrobial susceptibility profile of the isolates in Kurdistan province of Iran. Iran J Microbiol. 2021;13(1):65-73.
