1887

Abstract

The presence of in poultry and poultry products, including eggs, increases its potential to enter the food chain, resulting in foodborne diseases. In this context, eggshell colonization by staphylococci may represent a risk factor. This study aimed to investigate the contamination of rural eggshell by and to characterize the key features of the isolated strains.

Antibiotic resistance was assessed by disc diffusion. Resistant isolates were analysed by PCR for the identification of associated genetic determinants of resistance. PCR was also used to screen for the presence of genes coding for toxins, namely, , , , , and . The genetic characterization was extended by means of locus typing and typing.

34 were isolated. Macrolide- and tetracycline-resistant strains were prevalent. All strains were susceptible to oxacillin, cefoxitin and trimethoprim-sulfamethoxazole. PCR screening for genes encoding enterotoxins detected several virulence patterns, which, together with -typing and -locus typing, allowed cluster analysis and the description of novel clones.

Continuous monitoring of staphylococci is needed also in rural or natural settings. Increasing the number of samples and expanding the geographical region will be needed to further extend the significance of the study.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000540
2017-08-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/8/1196.html?itemId=/content/journal/jmm/10.1099/jmm.0.000540&mimeType=html&fmt=ahah

References

  1. Quarles CL, Gentry RF, Bressler GO. Bacterial contamination in poultry houses and its relationship to egg hatchability. Poult Sci 1970; 49:60–66 [View Article]
    [Google Scholar]
  2. Gentry RF, Quarles CL. The measurement of bacterial contamination on egg shells. Poult Sci 1972; 51:930–933 [View Article]
    [Google Scholar]
  3. Schoeni JL, Glass KA, Mcdermott JL, Wong AC. Growth and penetration of Salmonella enteritidis, Salmonella heidelberg and Salmonella typhimurium in eggs. Int J Food Microbiol 1995; 24:385–396 [View Article][PubMed]
    [Google Scholar]
  4. Barrow PA, Lovell MA. Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathol 1991; 20:335–348 [View Article][PubMed]
    [Google Scholar]
  5. Chaemsanit S, Akbar A, Anal AK. Isolation of total aerobic and pathogenic bacteria from table eggs and its contents. Food and Appl Bioscience J 2015; 3:1–9
    [Google Scholar]
  6. Abdullah IN. Isolation and identification of some bacterial isolates from table egg. J Vet Sci 2010; 3:59–67
    [Google Scholar]
  7. EFSA Panel on Biological Hazards (BIOHAZ) Scientific opinion on the public health risks of table eggs due to deterioration and development of pathogens. EFSA J 2014; 12:3782 [CrossRef]
    [Google Scholar]
  8. de Reu K, Grijspeerdt K, Heyndrickx M, Uyttendaele M, Herman L. Bacterial eggshell contamination in the egg production chain and in different housing systems. Zootec Int-World Poult J 2006; 22:20–21
    [Google Scholar]
  9. Baird-Parker AC. An improved diagnostic and selective medium for isolating coagulase positive staphylococci. J Appl Bacteriol 1962; 25:12–19 [View Article]
    [Google Scholar]
  10. 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[PubMed]
    [Google Scholar]
  11. European Committee on Antimicrobial Susceptibility Testing 2015; Breakpoint tables for interpretation of MICs and zone diameters version 5.0. www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_5.0_Breakpoint_Table_01.pdf
  12. Gómez-Sanz E, Torres C, Lozano C, Fernández-Pérez R, Aspiroz C et al. Detection, molecular characterization, and clonal diversity of methicillin-resistant Staphylococcus aureus CC398 and CC97 in Spanish slaughter pigs of different age groups. Foodborne Pathog Dis 2010; 7:1269–1277 [View Article][PubMed]
    [Google Scholar]
  13. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002; 70:631–641 [View Article][PubMed]
    [Google Scholar]
  14. Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L et al. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 2002; 70:4987–4996 [View Article][PubMed]
    [Google Scholar]
  15. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999; 37:3556–3563[PubMed]
    [Google Scholar]
  16. Severiano A, Carriço JA, Robinson DA, Ramirez M, Pinto FR. Evaluation of Jackknife and bootstrap for defining confidence intervals for pairwise agreement measures. PLoS One 2011; 6:e19539 [View Article][PubMed]
    [Google Scholar]
  17. Duran N, Ozer B, Duran GG, Onlen Y, Demir C. Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian J Med Res 2012; 135:389–396[PubMed]
    [Google Scholar]
  18. Sirmatel F, Zeyrek F, Erkmen O. Antibiotic resistance in nosocomial Staphylococcus strains with broth microdilution method. J Ankem 2004; 18:200–204
    [Google Scholar]
  19. Zmantar T, Chaieb K, Ben Abdallah F, Ben Kahla-Nakbi A, Ben Hassen A et al. Multiplex PCR detection of the antibiotic resistance genes in Staphylococcus aureus strains isolated from auricular infections. Folia Microbiol 2008; 53:357–362 [View Article][PubMed]
    [Google Scholar]
  20. Aarestrup FM, Agersł Y, Ahrens P, Jłrgensen JC, Madsen M et al. Antimicrobial susceptibility and presence of resistance genes in staphylococci from poultry. Vet Microbiol 2000; 74:353–364 [View Article][PubMed]
    [Google Scholar]
  21. Ullah F, Malik SA, Ahmed J, Ullah F, Shah SM et al. Investigation of the genetic basis of tetracycline resistance in Staphylococcus aureus from Pakistan. Trop J Pharm Res 2012; 6:925–931
    [Google Scholar]
  22. Francois P, Koessler T, Huyghe A, Harbarth S, Bento M et al. Rapid Staphylococcus aureus agr type determination by a novel multiplex real-time quantitative PCR assay. J Clin Microbiol 2006; 44:1892–1895 [View Article][PubMed]
    [Google Scholar]
  23. Fenner L, Widmer AF, Frei R. Molecular epidemiology of invasive methicillin-susceptible Staphylococcus aureus strains circulating at a Swiss University Hospital. Eur J Clin Microbiol Infect Dis 2008; 27:623–626 [View Article][PubMed]
    [Google Scholar]
  24. Olsen K, Sangvik M, Simonsen GS, Sollid JU, Sundsfjord A et al. Prevalence and population structure of Staphylococcus aureus nasal carriage in healthcare workers in a general population. The Tromsø Staph and skin study. Epidemiol Infect 2013; 141:143–152 [View Article][PubMed]
    [Google Scholar]
  25. Donker GA, Deurenberg RH, Driessen C, Sebastian S, Nys S et al. The population structure of Staphylococcus aureus among general practice patients from the Netherlands. Clin Microbiol Infect 2009; 15:137–143 [View Article][PubMed]
    [Google Scholar]
  26. Khademi F, Ghanbari F, Mellmann A, Najafzadeh MJ, Khaledi A. Phylogenetic relationships among Staphylococcus aureus isolated from clinical samples in Mashhad, Iran. J Infect Public Health 2016; 9:639–644 [View Article][PubMed]
    [Google Scholar]
  27. Abou Shady HM, Bakr AE, Hashad ME, Alzohairy MA. Staphylococcus aureus nasal carriage among outpatients attending primary health care centers: a comparative study of two cities in Saudi Arabia and Egypt. Braz J Infect Dis 2015; 19:68–76 [View Article][PubMed]
    [Google Scholar]
  28. Liu Y, Wang H, du N, Shen E, Chen H et al. Molecular evidence for spread of two major methicillin-resistant Staphylococcus aureus clones with a unique geographic distribution in Chinese hospitals. Antimicrob Agents Chemother 2009; 53:512–518 [View Article][PubMed]
    [Google Scholar]
  29. Cheng H, Yuan W, Zeng F, Hu Q, Shang W et al. Molecular and phenotypic evidence for the spread of three major methicillin-resistant Staphylococcus aureus clones associated with two characteristic antimicrobial resistance profiles in China. J Antimicrob Chemother 2013; 68:2453–2457 [View Article][PubMed]
    [Google Scholar]
  30. Goudarzi M, Fazeli M, Goudarzi H, Azad M, Seyedjavadi SS. Spa Typing of Staphylococcus aureus strains isolated from clinical specimens of patients with nosocomial infections in Tehran, Iran. Jundishapur J Microbiol 2016; 9:e35685 [View Article][PubMed]
    [Google Scholar]
  31. Grundmann H, Aanensen DM, van den Wijngaard CC, Spratt BG, Harmsen D et al. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med 2010; 7:e1000215 [View Article][PubMed]
    [Google Scholar]
  32. Rodriguez M, Hogan PG, Satola SW, Crispell E, Wylie T et al. Discriminatory indices of typing methods for epidemiologic analysis of contemporary Staphylococcus aureus strains. Medicine 2015; 94:e1534 [View Article][PubMed]
    [Google Scholar]
  33. Aarestrup FM, Wegener HC, Collignon P. Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti Infect Ther 2008; 6:733–750 [View Article][PubMed]
    [Google Scholar]
  34. Hatakka M, Björkroth KJ, Asplund K, Mäki-Petäys N, Korkeala HJ. Genotypes and enterotoxicity of Staphylococcus aureus isolated from the hands and nasal cavities of flight-catering employees. J Food Prot 2000; 63:1487–1491 [View Article][PubMed]
    [Google Scholar]
  35. Pinchuk IV, Beswick EJ, Reyes VE. Staphylococcal enterotoxins. Toxins 2010; 2:2177–2197 [View Article][PubMed]
    [Google Scholar]
  36. Argudín , Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2010; 2:1751–1773 [View Article][PubMed]
    [Google Scholar]
  37. Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014; 2014:827965 [View Article][PubMed]
    [Google Scholar]
  38. Hwang SY, Kim SH, Jang EJ, Kwon NH, Park YK et al. Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. Int J Food Microbiol 2007; 117:99–105 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000540
Loading
/content/journal/jmm/10.1099/jmm.0.000540
Loading

Data & Media loading...

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