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Journal of Integrative Agriculture  2016, Vol. 15 Issue (12): 2842-2847    DOI: 10.1016/S2095-3119(16)61368-0
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Genetic characterization of antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis cases in Northwest China
YANG Feng1*, WANG Qi2*, WANG Xu-rong1, WANG Ling1, LI Xin-pu1, LUO Jin-yin1, ZHANG Shi-dong1, LI Hong-sheng1
1 Key Laboratory of Veterinary Pharmaceutical Development, Ministry of Agriculture/Engineering & Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province/Lanzhou Institute of Husbandry and Pharmaceutical Sciences, Chinese Academy of Agricultural Sciences, Lanzhou 730050, P.R.China
2 State Key Laboratory of Applied Organic Chemistry, Lanzhou University, Lanzhou 730000, P.R.China
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Abstract      Staphylococcus aureus is the most common etiological pathogen of bovine mastitis. The resistant strains make the disease difficult to cure. The aim of this study was to characterize the genetic nature of the antimicrobial resistance in S. aureus cultured from bovine mastitis in Northwest China in 2014. A total of 44 S. aureus were isolated for antimicrobial resistance and resistance-related genes. Antimicrobial resistance was determined by disc diffusion and the corresponding resistance genes were detected by PCR. Phenotype indicated that S. aureus isolates were resistant to penicillin (84.09%), erythromycin (20.45%), tetracycline (15.91%), gentamicin (9.09%), tobramycin (6.82%), kanamycin (6.82%) and methicillin (2.27%). 9.09% of the S. aureus isolates were classified as multidrug resistant. In addition, genotypes showed that the isolates were resistant to rifampicin (100%, rpoB), penicillin (95.45%, blaZ), tetracycline (22.73%, tetK, tetM, alone or in combination), erythromycin (22.73%, ermB or ermC), gentamicin/tobramycin/kanamycin (2.27%, aacA-aphD), methicillin (2.27%, mecA) and vancomycin (2.27%, vanA). Resistance to tetracycline was attributed to the genes tetK and tetM (r=0.558, P<0.001). This study noted high-level geno- and phenotypic antimicrobial resistance in S. aureus isolates from bovine mastitis cases in Northwest China.
Keywords:  bovine mastitis        Staphylococcus aureus        antimicrobial resistance        phenotype        genotype  
Received: 30 December 2015   Accepted:

This study was supported by the Central Public-Interest Scientific Institution Basal Research Fund, China (1610322015007), the Key Technology R&D Program of China during the 12th Five-Year Plan period (2012BAD12B03) and the Natural Science Foundation of Gansu Province, China (145RJYA311).

Corresponding Authors:  LI Hong-sheng, Tel: +86-931-2164183, Fax: +86-931-2114180, E-mail:    
About author:  YANG Feng, E-mail:;

Cite this article: 

YANG Feng, WANG Qi, WANG Xu-rong, WANG Ling, LI Xin-pu, LUO Jin-yin, ZHANG Shi-dong, LI Hong-sheng. 2016. Genetic characterization of antimicrobial resistance in Staphylococcus aureus isolated from bovine mastitis cases in Northwest China. Journal of Integrative Agriculture, 15(12): 2842-2847.

Anthony R M, Connor A M, Power E G M, French G L. 1999. Use of the polymerase chain reaction for rapid detection of high-level mupirocin resistance in staphylococci. European Journal of Clinical Microbiology and Infectious Diseases, 18, 30–34.

Aubry-Damon H, Soussy C J, Courvalin P. 1998. Characterization of mutations in the rpoB gene that confer rifampin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 42, 2590–2594.

Bengtsson B, Unnerstad H E, Ekman T, Artursson K, Nilsson-Öst M, Waller K P. 2009. Antimicrobial susceptibility of udder pathogens from cases of acute clinical mastitis in dairy cows. Veterinary Microbiology, 136, 142–149.

Choi S M, Kim S H, Kim H J, Lee D G, Choi J H, Yoo J H, Kang J H, Shin W S, Kang M W. 2003. Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. Journal of Korean Medical Science, 18, 631–636.

CLSI (Clinical and Laboratory Standards Institute). 2010. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. CLSI document M 100-18, Clinical and Laboratory Standards Institute, Wayne, PA, USA.

Coelho S M O, Reinoso E, Pereira I A, Soares L C, Demo M, Bogni C, Souza M. 2009. Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis in Rio de Janeiro. Pesquisa Veterinaria Brasileira, 29, 369–374.

Croes S, Deurenberg R H, Boumans M L L, Beisser P S, Neef C, Stobberingh E E. 2009. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiology, 9, 229.

Dutka-Malen S, Evers S, Courvalin P. 1995. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. Journal of Clinical Microbiology, 33, 24–27.

El-Jakee J K, Atta N S, Samy A A, Bakry M A, Elgabry E A, Kandil M M, El-Said W A G. 2011. Antimicrobial resistance in clinical isolates of Staphylococcus aureus from bovine and human sources in Egypt. Global Veterinary, 7, 581–586.

Feßler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S. 2010. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. Journal of Antimicrobial Chemotherapy, 65, 619–625.

Finlay J E, Miller L A, Poupard J A. 1997. Interpretive criteria for testing susceptibility of staphylococci to mupirocin. Antimicrobial Agents and Chemotherapy, 41, 1137–1139.

Frey Y, Rodriguez J P, Thomann A, Schwendener S, Perreten V. 2013. Genetic characterization of antimicrobial resistance in coagulase-negative staphylococci from bovine mastitis milk. Journal of Dairy Science, 96, 2247–2257.

Gao J, Yu F Q, Luo L P, He J Z, Hou R G, Zhang H Q, Li S M, Su J L, Han B. 2012. Antibiotic resistance of Streptococcus agalactiae from cows with mastitis. Veterinary Journal, 194, 423–424.

Gow S P, Waldner C L, Harel J, Boerlin P. 2008. Associations between antimicrobial resistance genes in fecal generic Escherichia coli isolates from cow-calf herds in western Canada. Applied and Environmental Microbiology, 74, 3658–3666.

Güler L, Ok G, Gülcü K, Gülcü Y, Hadimli H H. 2005. Antimicrobial susceptibility and coagulase gene typing of Staphylococcus aureus isolated from bovine clinical mastitis cases in Turkey. Journal of Dairy Science, 88, 3149–3154.

Hammad A M, Shimamoto T. 2014. Genetic characterization of antibiotic resistance and virulence factors in Enterococcus spp. from Japanese retail ready-to-eat raw fish. Food Microbiology, 38, 62–66.

Hogan J, Smith K L. 2003. Coliform mastitis. Veterinary Research, 34, 507–519.

Jensen S O, Lyon B R. 2009. Genetics of antimicrobial resistance in Staphylococcus aureus. Future Microbiology, 4, 565–582.

Kumar R, Yadav B R, Anand S K, Singh R S. 2011. Molecular surveillance of putative virulence factors and antibiotic resistance in Staphylococcus aureus isolates recovered from intra-mammary infections of river buffaloes. Microbial Pathogenesis, 51, 31–38.

Magiorakos A P, Srinivasan A, Carey R B, Carmeli Y, Falagas M E, Giske C G, Harbarth S, Hindler J F, Kahlmeter G, Olsson-Liljequist B, Paterson D L, Rice L B, Stelling J, Struelens M J, Vatopoulos A, Weber J T, Monnet D L. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281

McDougall S, Hussein H, Petrovski K. 2014. Antimicrobial resistance in Staphylococcus aureus, Streptococcus uberis and Streptococcus dysgalactiae from dairy cows with mastitis. New Zealand Veterinary Journal, 62, 68–76.

Memon J, Yang Y, Kashifa J, Yaqoob M, Buriroa R, Soomroa J, Liping W, Hongjie F. 2013. Genotypes, virulence factors and antimicrobial resistance genes of Staphylococcus aureus isolated in bovine subclinical mastitis from Eastern China. Pakistan Veterinary Journal, 33, 486–491.

Moroni P, Pisoni G, Antonini M, Villa R, Boettcher P, Carli S. 2006. Short Communication: Antimicrobial drug susceptibility of Staphylococcus aureus from subclinical bovine mastitis in Italy. Journal of Dairy Science, 89, 2973–2976.

De Oliveira A P, Watts J L, Salmon S A, Aarestrup F M. 2000. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in europe and the united states. Journal of Dairy Science, 83, 855–862.

Olsen J E, Christensen H, Aarestrup F M. 2006. Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. Journal of Antimicrobial Chemotherapy, 57, 450–460.

O’Neill A J, Larsen A R, Henriksen A S, Chopra I. 2004. A fusidic acid-resistant epidemic strain of Staphylococcus aureus carries the fusB determinant, whereas fusA mutations are prevalent in other resistant isolates. Antimicrobial Agents and Chemotherapy, 48, 3594–3597.

Pantosti A, Sanchini A, Monaco M. 2007. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiology, 2, 323–334.

Pitkälä A, Haveri M, Pyörälä S, Myllys V, Honkanen-Buzalski T. 2004. Bovine mastitis in Finland 2001 - Prevalence, distribution of bacteria, and antimicrobial resistance. Journal of Dairy, 87, 2433–2441.

Rajala-Schultz P J, Smith K L, Hogan J S, Love B C. 2004. Antimicrobial susceptibility of mastitis pathogens from first lactation and older cows. Veterinary Microbiology, 102, 33–42.

Sharif A, Umer M, Muhammad G. 2009. Mastitis control in dairy production. Journal of Agriculture and Social Sciences, 5, 102–105.

Shi D, Hao Y, Zhang A, Wulan B, Fan X. 2010. Antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis in China. Transboundary and Emerging Diseases, 57, 221–224.

Skov R, Frimodt-Møller N, Espersen F. 2001. Correlation of MIC methods and tentative interpretive criteria for disk diffusion susceptibility testing using NCCLS methodology for fusidic acid. Diagnostic Microbiology and Infectious Disease, 40, 111–116.

Strommenger B, Kettlitz C, Werner G, Witte W. 2003. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. Journal of Clinical Microbiology, 41, 4089–4094.

Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L. 1996. Detection of erythromycin-resistant determinants by PCR. Antimicrobial Agents and Chemotherapy, 40, 2562–2566.

Tiwari H K, Sapkota D, Dad A K, Sen M R. 2009. Assessment of different tests to detect methicillin resistant Staphylococcus aureus. Southeast Asian Journal of Tropical Medicine and Public Health, 40, 801–806.

Unakal C G, Kaliwal B B. 2010. Prevalence and antibiotic susceptibility of Staphylococcus aureus from bovine mastitis. Veterinary World, 3, 65–67.

Wang D, Wang Z, Yan Z, Wu J, Ali T, Li J, Lv Y, Han B. 2015. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infection, Genetics and Evolution, 31, 9–16.
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