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Phenotypic and molecular characteristics of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in slaughterhouse pig-related workers and control workers in Guangdong Province, China

  • X. L. WANG (a1), L. LI (a1), S. M. LI (a1), J. Y. HUANG (a1), Y. P. FAN (a1), Z. J. YAO (a1), X. H. YE (a1) and S. D. CHEN (a1)...

Summary

Pig farmers and veterinarians have high prevalence of methicillin-resistant Staphylococcus aureus (MRSA) due to the occupational livestock exposure, while few reported this association on slaughterhouse workers. We conducted this cross-sectional study to explore the phenotypic and molecular characteristics of S. aureus and MRSA in slaughterhouse pig-related workers and control workers in Guangdong Province, China. Participants were interviewed and provided two nasal swabs. Swabs were tested for S. aureus, and isolates were further tested for antimicrobial susceptibility, virulence genes and multi-locus sequence typing. Compared with control workers, pig-related workers have significantly higher prevalence of MRSA carriage (adjusted odd ratio (aOR) 3·70, 95% CI 1·63–8·40). The proportions of MRSA resistant to clindamycin, erythromycin, tetracycline or chloromycetin were significantly higher in pig-related workers than in control workers. The predominant phenotypes of S. aureus were resistant to penicillin, clindamycin, erythromycin and tetracycline. Three MRSA CC9 isolates with livestock-associated characteristics (resistance to tetracycline and absence of immune evasion cluster (IEC) genes) were detected in pig-related workers but not in control workers. For human-associated CCs (CC7, CC59, CC6, and CC188), there was no significant difference in IEC profile or antimicrobial resistance between the groups. These findings reveal that there may be a potential risk for livestock-to-human transmission of LA-MRSA and human-to-human transmission of human-associated MRSA.

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Corresponding author

*Author for correspondence: S. Chen, Guangdong Pharmaceutical University, 283# Jianghai Dadao, Haizhu District, Guangzhou 510310, China. (Email: chensidong1@126.com)

References

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1. Graveland, H, et al. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology 2011; 301: 630634.
2. Huang, E, et al. Detection of livestock-associated methicillin-resistant Staphylococcus aureus among swine workers in Romania. Journal of Infection and Public Health 2014; 7: 323332.
3. Hau, SJ, et al. Comparative prevalence of immune evasion complex genes associated with β-hemolysin converting bacteriophages in MRSA ST5 isolates from swine, swine facilities, humans with swine contact, and humans with no swine contact. PLoS ONE 2015; 10: e142832.
4. Huijsdens, XW, et al. Community-acquired MRSA and pig-farming. Annals of Clinical Microbiology and Antimicrobials 2006; 5: 26.
5. Vanderhaeghen, W, et al. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary Microbiology 2010; 144: 166171.
6. Mulders, MN, et al. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiology and Infection 2010; 138: 743.
7. Chuang, Y, Huang, Y. Livestock-associated meticillin-resistant Staphylococcus aureus in Asia: an emerging issue? International Journal of Antimicrobial Agents 2015; 45: 334340.
8. Cuny, C, et al. Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS ONE 2009; 4: e6800.
9. Smith, TC, et al. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS ONE 2009; 4: e4258.
10. Garcia-Graells, C, et al. Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398. Epidemiology and Infection 2012; 140: 383389.
11. Van Cleef, BA, et al. High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands. Epidemiology and Infection 2010; 138: 756763.
12. Normanno, G, et al. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy. Food Microbiology 2015; 51: 5156.
13. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 23nd informational supplement M100-S23. Wayne, PA: CLSI, 2013.
14. Magiorakos, AP, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection 2012; 18: 268281.
15. Zhang, K, et al. Novel multiplex PCR assay for simultaneous identification of community-associated methicillin-resistant Staphylococcus aureus strains USA300 and USA400 and detection of mecA and Panton–Valentine leukocidin genes, with discrimination of Staphylococcus aureus from coagulase-negative staphylococci. Journal of Clinical Microbiology 2008; 46: 11181122.
16. Enright, MC, et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus . Journal of Clinical Microbiology 2000; 38: 10081015.
17. van Wamel, WJ, et al. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. Journal of Bacteriology 2006; 188: 13101315.
18. Moon, DC, et al. Identification of livestock-associated methicillin-resistant staphylococcus aureus isolates in Korea and molecular comparison between isolates from animal carcasses and slaughterhouse workers. Foodborne Pathogens and Disease 2015; 12: 327334.
19. Boost, M, et al. Colonization of butchers with livestock-associated methicillin-resistant Staphylococcus aureus . Zoonoses and Public Health 2013; 60: 572576.
20. Leibler, JH, et al. Staphylococcus aureus nasal carriage among beef packing workers in a Midwestern United States slaughterhouse. PLoS ONE 2016; 11: e148789.
21. Oppliger, A, et al. Antimicrobial resistance of staphylococcus aureus strains acquired by pig farmers from pigs. Applied and Environmental Microbiology 2012; 78: 80108014.
22. Neyra, RC, et al. Multidrug-resistant and methicillin-resistant Staphylococcus aureus (MRSA) in hog slaughter and processing plant workers and their community in North Carolina (USA). Environmental Health Perspectives 2014; 122: 471477.
23. Ye, X, et al. Frequency-risk and duration-risk relations between occupational livestock contact and methicillin-resistant Staphylococcus aureus carriage among workers in Guangdong, China. American Journal of Infection Control 2015; 43: 676681.
24. Lo, YP, et al. Molecular characterization and clonal genetic diversity of methicillin-resistant Staphylococcus aureus of pig origin in Taiwan. Comparative Immunology Microbiology and Infectious Diseases 2012; 35: 513521.
25. Cui, S, et al. Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. Journal of Antimicrobial Chemotherapy 2009; 64: 680683.
26. Price, LB, et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 2012; 3.
27. Uhlemann, AC, et al. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. mBio 2012; 3.
28. Narvaez-Bravo, C, et al. Prevalence of methicillin-resistant Staphylococcus aureus in Canadian commercial pork processing plants. Journal of Applied Microbiology 2016; 120: 770780.
29. Spoor, LE, et al. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus . mBio 2013; 4: e313e356.
30. McCarthy, AJ, Lindsay, JA. Staphylococcus aureus innate immune evasion is lineage-specific: a bioinfomatics study. Infection, Genetics and Evolution 2013; 19: 714.
31. Fan, Y, et al. Potential relationship between phenotypic and molecular characteristics in revealing livestock-associated Staphylococcus aureus in Chinese humans without occupational livestock contact. Frontiers in Microbiology 2016; 7: 1517.
32. Liu, H, et al. The carriage of the serine-aspartate repeat protein-encoding sdr genes among Staphylococcus aureus lineages. Brazilian Journal of Infectious Diseases 2015; 19: 498502.
33. Yu, F, et al. Antimicrobial susceptibility, virulence determinant carriage and molecular characteristics of Staphylococcus aureus isolates associated with skin and soft tissue infections. Brazilian Journal of Infectious Diseases 2015; 19: 614622.

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