Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-18T21:01:45.585Z Has data issue: false hasContentIssue false
  • English
  • Français

Resistance to Zinc and Cadmium in Staphylococcus aureus of Human and Animal Origin

Published online by Cambridge University Press:  10 May 2016

Rajeshwari Nair ,
Dipendra Thapaliya ,
Yutao Su  and
Tara C. Smith
Rajeshwari Nair
Affiliation:
Center for Emerging Infectious Diseases, College of Public Health, University of Iowa, Iowa City, Iowa Department of Epidemiology, College of Public Health, University of Iowa, Iowa City, Iowa
Dipendra Thapaliya
Affiliation:
Department of Biostatistics, Environmental Health Sciences and Epidemiology, College of Public Health, Kent State University, Kent, Ohio
Yutao Su
Affiliation:
Center for Emerging Infectious Diseases, College of Public Health, University of Iowa, Iowa City, Iowa
Tara C. Smith
Affiliation:
Center for Emerging Infectious Diseases, College of Public Health, University of Iowa, Iowa City, Iowa Department of Biostatistics, Environmental Health Sciences and Epidemiology, College of Public Health, Kent State University, Kent, Ohio
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Objective.

Studies conducted in Europe have observed resistance to trace metals such as zinc chloride and copper sulfate in livestock-associated Staphylococcus aureus. This study was conducted to determine the prevalence of zinc and cadmium resistance in S. aureus isolated in the United States.

Design.

Cross-sectional study of convenience sample of S. aureus isolates.

Participants.

Three hundred forty-nine S. aureus isolates, including methicillin-resistant S. aureus (MRSA) and methicillin-susceptible S. aureus (MSSA) obtained from human, swine, and retail meat were included in the sample set.

Methods.

Polymerase chain reaction was used to test for the presence of genes for zinc and cadmium resistance (czrC), methicillin resistance (mecA), and staphylococcal complement inhibitor (scn). Antibiotic susceptibility of isolates was tested using the broth microdilution method. Data were analyzed using the multivariable logistic regression method.

Results.

Twenty-nine percent (102/349) of S. aureus isolates were czrC positive. MRSA isolates were more likely to be czrC positive compared to MSSA (MRSA czrC positive: 12/61, 19.6%; MSSA czrC positive: 12/183, 6.6%). After adjustment for oxacillin and clindamycin susceptibility in analysis, multidrug-resistant S. aureus was observed to have low odds of being czrC positive (P = .03). The odds of being czrC positive were observed to be significantly high in tetracycline-resistant S. aureus isolated from noninfection samples (P = .009) and swine (P < .0001).

Conclusions.

Resistance to zinc and cadmium was observed to be associated with MRSA, a finding consistently observed in European studies. Prolonged exposure to zinc in livestock feeds and fertilizers could propagate resistance to the metal ion, thereby hindering use of zinc-based topical agents in treating S. aureus infections.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 35 , Issue S3: Preventing Healthcare–Associated Infections: Results and Lessons Learned from AHRQ's HAI Program , October 2014 , pp. S32 - S39
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2014

References

1. Dukic, VM, Lauderdale, DS, Wilder, J, Daum, RS, David, MZ. Epidemics of community-associated methicillin-resistant Staph-ylococcus aureus in the United States: a meta-analysis. PLoS ONE 2013;8:e52722.Google Scholar
2. Eells, SJ, McKinnell, JA, Wang, AA, et al. A comparison of clinical outcomes between healthcare-associated infections due to community-associated methicillin-resistant Staphylococcus aureus strains and healthcare-associated methicillin-resistant S. aureus strains. Epidemiol Infect 2012:1–9.Google ScholarPubMed
3. Enright, MC, Day, NP, Davies, CE, Peacock, SI, Spratt, BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus . J Clin Microbiol 2000;38:1008–1015.CrossRefGoogle ScholarPubMed
4. Robinson, DA, Enright, MC. Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus . Clin Microbiol Infect 2004;10:92–97.Google Scholar
5. Smith, TC, Pearson, N. The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis 2011;11:327–339.Google Scholar
6. Stegger, M, Lindsay, JA, Sorum, M, Gould, KA, Skov, R. Genetic diversity in CC398 methicillin-resistant Staphylococcus aureus isolates of different geographical origin. Clin Microbiol Infect 2010;16:1017–1019.Google Scholar
7. Verkade, E, Kluytmans, J. Livestock-associated Staphylococcus aureus CC398: animal reservoirs and human infections. Infect Genet Evol 2014;21:523–530.CrossRefGoogle ScholarPubMed
8. Graveland, H, Duim, B., van Duijkeren, E, Heederik, D, Wagenaar, JA. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 2011;301:630–634.Google Scholar
9. Agerso, Y, Hasman, H, Cavaco, LM, Pedersen, K, Aarestrup, FM. Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Vet Microbiol 2012;157:246–250.Google Scholar
10. O'Brien, AM, Hanson, BM, Farina, SA, et al. MRSA in conventional and alternative retail pork products. PLoS ONE 2012;7: e30092.CrossRefGoogle ScholarPubMed
11. Aarestrup, FM, Cavaco, L, Hasman, H. Decreased susceptibility to zinc chloride is associated with methicillin resistant Staphylococcus aureus CC398 in Danish swine. Vet Microbiol 2010;142: 455–457.Google Scholar
12. de Neeling, AJ, van den Broek, MJ, Spalburg, EC, et al. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 2007;122:366–372.Google Scholar
13. Amachawadi, RG, Shelton, NW, Shi, X, et al. Selection of fecal enterococci exhibiting tcrB-mediated copper resistance in pigs fed diets supplemented with copper. Appl Environ Microbiol 2011;77:5597–5603.Google Scholar
14. Aarestrup, FM, Hasman, H. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet Microbiol 2004;100:83–89.Google Scholar
15. Hill, GM, Cromwell, GL, Crenshaw, TD, et al. Growth promotion effects and plasma changes from feeding high dietary concentrations of zinc and copper to weanling pigs (regional study). J Anim Sci 2000;78:1010–1016.CrossRefGoogle ScholarPubMed
16. Kuroda, M, Hayashi, H, Ohta, T. Chromosome-determined zinc-responsible operon czr in Staphylococcus aureus strain 912. Microbiol Immunol 1999;43:115–125.Google Scholar
17. Cavaco, LM, Hasman, H, Stegger, M, et al. Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob Agents Chemother 2010;54:3605–3608.Google Scholar
18. Ito, T, Katayama, Y, Asada, K, et al. Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus . Antimicrob Agents Chemother 2001;45:1323–1336.Google Scholar
19. Poston, SM, Li Saw Hee, FL. Genetic characterisation of resistance to metal ions in methicillin-resistant Staphylococcus aureus: elimination of resistance to cadmium, mercury and tetracycline with loss of methicillin resistance. J Med Microbiol 1991;34:193–201.Google Scholar
20. Vandendriessche, S, Vanderhaeghen, W, Larsen, J, et al. High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSA CC398. J Antimicrob Chemother 2014;69:355–362.Google Scholar
21. Cavaco, LM, Hasman, H, Aarestrup, FM. Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol 2011;150:344–348.CrossRefGoogle ScholarPubMed
22. US Department of Agriculture. Quarterly Hogs and Pigs. Washington, DC: National Agricultural Statistics Service, Agricultural Statistics Board; 2013.Google Scholar
23. Smith, TC, Gebreyes, WA, Abley, MJ, et al. Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS ONE 2013;8: e63704.CrossRefGoogle ScholarPubMed
24. Dressier, AE, Scheibel, RP, Wardyn, S, et al. Prevalence, antibiotic resistance and molecular characterisation of Staphylococcus aureus in pigs at agricultural fairs in the USA. Vet Ree 2012; 170:495.Google Scholar
25. Wardyn, SE, Kauffman, LK, Smith, TC. Methicillin-resistant Staphylococcus aureus in central Iowa wildlife, J Wildl Dis 2012; 48:1069–1073.Google Scholar
26. Hanson, BM, Dressier, AE, Harper, AL, et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health 2011;4: 169–174.Google Scholar
27. Wardyn, SE, Forshey, BM, Smith, TC. High prevalence of Panton-Valentine leukocidin among methicillin-sensitive Staphylococcus aureus colonization isolates in rural Iowa. Microb Drug Resist 2012;18:427–433.CrossRefGoogle ScholarPubMed
28. Mellmann, A, Weniger, T, Berssenbrugge, C, et al. Characterization of clonal relatedness among the natural population of Staphylococcus aureus strains by using spa sequence typing and the BURP (based upon repeat patterns) algorithm, J Clin Microbiol 2008;46:2805–2808.CrossRefGoogle ScholarPubMed
29. Hasman, H, Moodley, A, Guardabassi, L, Stegger, M, Skov, RL, Aarestrup, FM. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol 2010; 141:326–331.Google Scholar
30. Lozano, C, Gomez-Sanz, E, Benito, D, Aspiroz, C, Zarazaga, M, Torres, C. Staphylococcus aureus nasal carriage, virulence traits, antibiotic resistance mechanisms, and genetic lineages in healthy humans in Spain, with detection of CC398 and CC97 strains. Int J Med Microbiol 2011;301:500–505.Google Scholar
31. Price, LB, Stegger, M, Hasman, H, et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 2012, e00305-ll.Google Scholar
32. Shopsin, B, Gomez, M, Montgomery, SO, et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999;37:3556–3563.Google Scholar
33. Mellmann, A, Weniger, T, Berssenbrugge, C, et al. Based Upon Repeat Pattern (BURP): an algorithm to characterize the long-term evolution of Staphylococcus aureus populations based on spa polymorphisms. BMC Microbiol 2007;7:98.Google Scholar
34. Bosgelmez-Tinaz, G, Ulusoy, S, Aridogan, B, Coskun-Ari F. Evaluation of different methods to detect oxacillin resistance in Staphylococcus aureus and their clinical laboratory utility. Eur J Clin Microbiol Infect Dis 2006;25:410–412.Google Scholar
35. Clinical Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing—Twenty-Second Informational Supplement. Wayne, PA: CLSI; 2012. CLSI document M100-S22.Google Scholar
36. Magiorakos, AP, Srinivasan, A, Carey, RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268–281.Google Scholar
37. Katouli, M, Melin, L, Jensen-Waern, M, Wallgren, P, Mollby, R. The effect of zinc oxide supplementation on the stability of the intestinal flora with special reference to composition of coliforms in weaned pigs. J Appl Microbiol 1999;87:564–573.Google Scholar
38. Kansas State University College of Agriculture. Swine nutrition guide. http://www.asi.k-state.edu/species/swine/research-and-extension/swine-nutrition-guide.html.Google Scholar