1887

Abstract

The genus is known to possess the capacity to acquire and disseminate antimicrobial resistant determinants alongside the ability to produce various virulence genes that enables it to establish infections. We assessed the prevalence and antibiogram profiles of spp. in faecal samples of dairy cattle. Faecal swab samples were collected from 400 dairy cattle from two commercial cattle farms in two rural communities in the Eastern Cape, South Africa. Confirmation of enterococci isolates was carried out by PCR targeting of the gene. Species delineation was by species-specific primers targeting the superoxide dismutase ( A) gene in a multiplex PCR assay. Isolates were screened for the presence of the following virulence genes (, E, , A, A and E) and antimicrobial resistance determinants to erythromycin, vancomycin and streptomycin were evaluated molecularly. A total of 340 isolates were confirmed as belonging to the genus . Species distribution among the isolates consisted of (52.94 %) and (23.53 %) in preponderance compared to the three other species, namely (8.8 %), (8.6 %) and (5.9 %). All were resistant to vancomycin, while 99 % showed resistance to aminoglycoside and 94 % to macrolide. Three virulence genes (, E and ) were detected in almost all the confirmed isolates. The resistance determinants B (19.7 %), C1 (25 %), C2/3 (26.3 %) B (40.29 %) and A (50.88 %) were detected among the isolates. A high prevalence of multidrug-resistant enterococci isolates was detected in this study and the genetic repertoire to survive in the presence of antimicrobial agents was present in these organisms.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000275
2016-07-01
2020-09-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/7/641.html?itemId=/content/journal/jmm/10.1099/jmm.0.000275&mimeType=html&fmt=ahah

References

  1. Aslam M., Diarra M. S., Checkley S., Bohaychuk V., Masson L.. 2012; Characterization of antimicrobial resistance and virulence genes in Enterococcus spp. isolated from retail meats in Alberta, Canada. Int J Food Microbiol156:222–230 [CrossRef][PubMed]
    [Google Scholar]
  2. Bai J., Paddock Z. D., Shi X., Li S., An B., Nagaraja T. G.. 2012; Applicability of a multiplex PCR to detect the seven major Shiga toxin-producing Escherichia coli based on genes that code for serogroup-specific O-antigens and major virulence factors in cattle feces. Foodborne Pathog Dis9:541–548 [CrossRef][PubMed]
    [Google Scholar]
  3. Boerlin P., Wissing A., Aarestrup F. M., Frey J., Nicolet J.. 2001; Antimicrobial growth promoter ban and resistance to macrolides and vancomycin in enterococci from pigs. J Clin Microbiol39:4193–4195 [CrossRef][PubMed]
    [Google Scholar]
  4. Bonten M. J., Willems R., Weinstein R. A.. 2001; Vancomycin-resistant enterococci: why are they here, and where do they come from?. Lancet Infect Dis1:314–325 [CrossRef][PubMed]
    [Google Scholar]
  5. Brtkova A., Bujdakova H.. 2009; Antibiotic resistance in Enterococcus isolates from poultry swabs in Slovakia. J Food Nutr Res48:121–128
    [Google Scholar]
  6. Byappanahalli M. N., Nevers M. B., Korajkic A., Staley Z. R., Harwood V. J.. 2012; Enterococci in the environment. Microbiol Mol Bio Rev76:685–706 [CrossRef]
    [Google Scholar]
  7. Casey J. A., Curriero F. C., Cosgrove S. E., Nachman K. E., Schwartz B. S.. 2013; High-density livestock operations, crop field application of manure, and risk of community-associated methicillin-resistant Staphylococcus aureus infection in Pennsylvania. JAMA Intern Med173:1980–1990 [CrossRef][PubMed]
    [Google Scholar]
  8. Clinical and Laboratory Standards Institute 2014; Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement.
  9. Diarra M. S., Silversides F. G., Diarrassouba F., Pritchard J., Masson L., Brousseau R., Bonnet C., Delaquis P., Bach S. et al. 2007; Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Appl Environ Microbiol73:6566–6576 [CrossRef][PubMed]
    [Google Scholar]
  10. Diarra M. S., Rempel H., Champagne J., Masson L., Pritchard J., Topp E.. 2010; Distribution of antimicrobial resistance and virulence genes in Enterococcus spp. and characterization of isolates from broiler chickens. Appl Environ Microbiol76:8033–8043 [CrossRef][PubMed]
    [Google Scholar]
  11. Diarrassouba F., Diarra M. S., Bach S., Delaquis P., Pritchard J., Topp E., Skura B. J.. 2007; Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J Food Prot70:1316–1327[PubMed][Crossref]
    [Google Scholar]
  12. Dierikx C. M., van Duijkeren E., Schoormans A. H., van Essen-Zandbergen A., Veldman K., Kant A., Huijsdens X. W., van der Zwaluw K., Wagenaar J. A. et al. 2012; Occurrence and characteristics of extended-spectrum-β -lactamase- and AmpC-producing clinical isolates derived from companion animals and horses. J Antimicrob Chemother67:1368–1374 [CrossRef][PubMed]
    [Google Scholar]
  13. Ding G. C., Radl V., Schloter-Hai B., Jechalke S., Heuer H., Smalla K., Schloter M.. 2014; Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One9:e92958 [CrossRef][PubMed]
    [Google Scholar]
  14. Donabedian S. M., Thal L. A., Hershberger E., Perri M. B., Chow J. W., Bartlett P., Jones R., Joyce K., Rossiter S. et al. 2003; Molecular characterization of gentamicin-resistant Enterococci in the United States: evidence of spread from animals to humans through food. J Clin Microbiol41:1109–1113[PubMed][Crossref]
    [Google Scholar]
  15. Eaton T. J., Gasson M. J.. 2001; Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol67:1628–1635 [CrossRef][PubMed]
    [Google Scholar]
  16. Freitas A. R., Coque T. M., Novais C., Hammerum A. M., Lester C. H., Zervos M. J., Donabedian S., Jensen L. B., Francia M. V. et al. 2011; Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol49:925–931 [CrossRef][PubMed]
    [Google Scholar]
  17. Garcia-Migura L., Pleydell E., Barnes S., Davies R. H., Liebana E.. 2005; Characterization of vancomycin-resistant Enterococcus faecium isolates from broiler poultry and pig farms in England and Wales. J Clin Microbiol43:3283–3289 [CrossRef][PubMed]
    [Google Scholar]
  18. Gaze W. H., Krone S. M., Larsson D. G. J., Li X., Robinson J. A., Simonet P., Smalla K., Timinouni M., Topp E.. 2013; Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg Infect Dis19:[Crossref]
    [Google Scholar]
  19. Geenen P. L., Graat E. A., Haenen A., Hengeveld P. D., Van Hoek A. H., Huijsdens X. W., Kappert C. C., Lammers G. A., Van Duijkeren E. et al. 2013; Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiol Infect141:1099–1108 [CrossRef][PubMed]
    [Google Scholar]
  20. Giridhara Upadhyaya P. M., Ravikumar K. L., Umapathy B. L.. 2009; Review of virulence factors of enterococcus: an emerging nosocomial pathogen. Indian J Med Microbiol27:301 [CrossRef][PubMed]
    [Google Scholar]
  21. Hamelin K., Bruant G., El-Shaarawi A., Hill S., Edge T. A., Fairbrother J., Harel J., Maynard C., Masson L. et al. 2007; Occurrence of virulence and antimicrobial resistance genes in Escherichia coli isolates from different aquatic ecosystems within the St. Clair River and Detroit River areas. Appl Environ Microbiol73:477–484 [CrossRef][PubMed]
    [Google Scholar]
  22. Hancock L. E., Gilmore M. S.. 2006; Pathogenicity of enterococci. In Gram-Positive Pathogens, 2nd edn. pp.299–311 Edited by Fischetti V. A., Novick R. P., Ferretti J. J., Portnoy D. A., Rood J. I.. Washington, DC: ASM Press;[Crossref]
    [Google Scholar]
  23. Hershberger E., Oprea S. F., Donabedian S. M., Perri M., Bozigar P., Bartlett P., Zervos M. J.. 2005; Epidemiology of antimicrobial resistance in enterococci of animal origin. J Antimicrob Chemother55:127–130 [CrossRef][PubMed]
    [Google Scholar]
  24. Heuer H., Schmitt H., Smalla K.. 2011; Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol14:236–243 [CrossRef][PubMed]
    [Google Scholar]
  25. Heuer H., Solehati Q., Zimmerling U., Kleineidam K., Schloter M., Müller T., Focks A., Thiele-Bruhn S., Smalla K. et al. 2011; Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl Environ Microbiol77:2527–2530 [CrossRef][PubMed]
    [Google Scholar]
  26. Huijsdens X. W., van Dijke B. J., Spalburg E., van Santen-Verheuvel M. G., Heck M. E., Pluister G. N., Voss A., Wannet W. J., de Neeling A. J.. 2006; Community-acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob5:26 [CrossRef][PubMed]
    [Google Scholar]
  27. Iweriebor B. C., Iwu C. J., Obi L. C., Nwodo U. U., Okoh A. I., Obi C. L., Nwodo C. L.. 2015a; Multiple antibiotic resistances among Shiga toxin producing Escherichia coli O157 in feces of dairy cattle farms in Eastern Cape of South Africa. BMC Microbiol15:213 [CrossRef][PubMed]
    [Google Scholar]
  28. Iweriebor B. C., Obi L. C., Okoh A. I.. 2015b; Virulence and antimicrobial resistance factors of Enterococcus spp. isolated from fecal samples from piggery farms in Eastern Cape, South Africa. BMC Microbiol15:136 [CrossRef][PubMed]
    [Google Scholar]
  29. Iwu C. J., Iweriebor B. C., Obi C. L., Okoh A. I.. 2015; Prevalence and virulence factors of Escherichia coli serogroups O157:H7, O26 and O145 shed by swine in Nkonkobe. Compar Immunol Microbiol Infect Dis44:48–53[Crossref]
    [Google Scholar]
  30. Jackson C. R., Fedorka-Cray P. J., Barrett J. B.. 2004; Use of a genus- and species-specific multiplex PCR for identification of enterococci. J Clin Microbiol42:3558 [CrossRef][PubMed]
    [Google Scholar]
  31. Jackson C. R., Fedorka-Cray P. J., Barrett J. B., Hiott L. M., Woodley T. A.. 2007; Prevalence of streptogramin resistance in enterococci from animals: identification of vatD from animal sources in the USA. Int J Antimicrob Agents30:60–66 [CrossRef][PubMed]
    [Google Scholar]
  32. Jamet E., Akary E., Poisson M. A., Chamba J. F., Bertrand X., Serror P.. 2012; Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol31:191–198 [CrossRef][PubMed]
    [Google Scholar]
  33. Jung W. K., Lim J. Y., Kwon N. H., Kim J. M., Hong S. K., Koo H. C., Kim S. H., Park Y. H.. 2007; Vancomycin-resistant enterococci from animal sources in Korea. Int J Food Microbiol113:102–107 [CrossRef][PubMed]
    [Google Scholar]
  34. Ke D., Picard F. J., Martineau F., Ménard C., Roy P. H., Ouellette M., Bergeron M. G.. 1999; Development of a PCR assay for rapid detection of enterococci. J Clin Microbiol37:3497–3503[PubMed]
    [Google Scholar]
  35. Klibi N., Aouini R., Borgo F., Ben Said L., Ferrario C., Dziri R., Boudabous A., Torres C., Ben Slama K, Said L. B. et al. 2015; Antibiotic resistance and virulence of faecal enterococci isolated from food-producing animals in Tunisia. Ann Microbiol65:695–702 [CrossRef]
    [Google Scholar]
  36. Laverde-Gomez J. A., Van S. W., Freitas A. R., Coque T. M., Weaver K. E., Francia M. V., Witte W., Werner G. A.. 2010; A multi-resistance mega-plasmid pLG1 bearing a hyl(Efm) genomic island in hospital Enterococcus faecium isolates. Int J Med Microbiol23:345–352
    [Google Scholar]
  37. Macovei L., Zurek L.. 2007; Influx of enterococci and associated antibiotic resistance and virulence genes from ready-to-eat food to the human digestive tract. Appl Environ Microbiol73:6740–6747 [CrossRef][PubMed]
    [Google Scholar]
  38. Mannu L., Paba A., Daga E., Comunian R., Zanetti S., Duprè I., Sechi L. A.. 2003; Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. Int J Food Microbiol88:291–304[PubMed][Crossref]
    [Google Scholar]
  39. Nam S., Kim M. J., Park C., Park J. G., Maeng P. J., Lee G. C.. 2013; Detection and genotyping of vancomycin-resistant Enterococcus spp. by multiplex polymerase chain reaction in Korean aquatic environmental samples. Int J Hyg Environ Health216:421–427 [CrossRef][PubMed]
    [Google Scholar]
  40. Roberts M. C., Sutcliffe J., Courvalin P., Jensen L. B., Rood J., Seppala H.. 1999; Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob Agents Chemother43:2823–2830[Crossref]
    [Google Scholar]
  41. Shankar N., Baghdayan A. S., Gilmore M. S.. 2002; Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis . Nature417:746–750 [CrossRef][PubMed]
    [Google Scholar]
  42. Shankar V., Baghdayan A. S., Huycke M. M., Lindahl G., Gilmore M. S.. 1999; Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect Immun67:193–200[PubMed]
    [Google Scholar]
  43. Simjee S., Jensen L. B., Donabedian S. M., Zervos M. J.. 2006; Enterococcus. In Antimicrobial Resistance in Bacteria of Animal Origin , pp.315–328 Edited by Aarestrup F. M.. Washington, DC: ASM Press;
    [Google Scholar]
  44. Sørensen T. L., Blom M., Monnet D. L., Frimodt-Møller N., Poulsen R. L., Espersen F.. 2001; Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N Engl J Med345:1161–1166 [CrossRef][PubMed]
    [Google Scholar]
  45. Sujatha S., Praharaj I.. 2012; Glycopeptide resistance in gram-positive cocci: a review. Interdiscip Perspect Infect Dis2012: [CrossRef][PubMed]
    [Google Scholar]
  46. Templer S., Baumgartner A.. 2007; Enterococci from appenzeller and schabziger raw milk cheese: antibiotic resistance, virulence factors, and persistence of particular strains in the products. J Food Protect70:450–455[Crossref]
    [Google Scholar]
  47. Tendolkar P. M., Baghdayan A. S., Shankar N.. 2005; The N-terminal domain of enterococcal surface protein, Esp, is sufficient for Esp-mediated biofilm enhancement in Enterococcus faecalis . J Bacteriol187:6213–6222 [CrossRef][PubMed]
    [Google Scholar]
  48. Valenzuela A. S., Omar N. B., Abriouel H., López R. L., Veljovic K., Cañamero M. M., Topisirovic M. K. L., Gálvez A.. 2009; Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control20:381–385 [CrossRef]
    [Google Scholar]
  49. Wegener H. C., Aarestrup F. M., Jensen L. B., Hammerum A. M., Bager F.. 1999; Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg Infect Dis5:329–335 [CrossRef][PubMed]
    [Google Scholar]
  50. Werner G., Dahl K. H., Willems R. J.. 2006; Composite elements encoding antibiotic resistance in Enterococcus faecium and Enterococcus faecalis . In Drug Resistance in Enterococci: Epidemiology and Molecular Markers , pp.157–208 Edited by Kobayashi N.. Trivandrum, Kerala: Research Signpost, Fort P.O;
    [Google Scholar]
  51. Werner G., Fleige C., Geringer U., van Schaik W., Klare I., Witte W., Van S. W.. 2011; IS element IS16 as a molecular screening tool to identify hospital-associated strains of Enterococcus faecium . BMC Infect Dis11:80–92 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000275
Loading
/content/journal/jmm/10.1099/jmm.0.000275
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error