Species Variety, Antibiotic Susceptibility Patterns and Prevalence of Enterotoxin Genes in Staphylococci Isolated from Foodstuff in Central Iran
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Abstract
Background: The presence and diversity of Staphylococcus species and their enterotoxin-encoding genes in foodstuffs have not been comprehensively studied in some developing countries. This study aimed to assess the frequency of Staphylococcus spp. and their related virulence factors in foodstuffs in Isfahan, Iran.
Methods: Overall, 139 foodstuff samples, collected from Isfahan City (center of Iran) from Sep 2015 to Oct 2016, were processed for the presence of Staphylococcus spp. using standard bacteriological procedures and sequence analysis of 16S rRNA gene. Antimicrobial susceptibilities and prevalence of mecA and toxin-encoded genes (sea, seb, sed, see and tsst1) were tested for all of the Staphylococcal isolates.
Results: Forty-four Gram-positive cocci were recovered from 139 dairy and meat samples. The most prevalent species were S. vitulinus 25.0% (11/44) and S. aureus 20.5% (9/44); respectively. The most prevalent antimicrobial resistance was noted towards penicillin, cefoxitin and tetracycline. The sec, sea, see and tsst1 genes were found in 19%, 9.5%, 3.5%, and 3.5% of the isolates, respectively.
Conclusion: Numerous virulence factors were detected in different Staphylococcus spp. isolated from foodstuffs, more attention should be paid to the presence of the bacteria. Proper hygienic and management practices should be considered in order to increase food safety and prevent extra treatment costs.
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14. Jeon Y-S, Chung H, Park S et al (2005). jPHYDIT: a JAVA-based integrated environment for molecular phylogeny of ribosomal RNA sequences. Bioinformatics, 21 (14): 3171-73.
15. McClure J-A, Conly JM, Lau V et al (2006). Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J Clin Microbiol, 44 (3): 1141-44.
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17. Monday SR, Bohach GA (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol, 37 (10): 3411-14.
18. Dinges MM, Orwin PM, Schlievert PM (2000). Exotoxins of Staphylococcus aureus. Clin Microbiol Rev, 13 (1): 16-34.
19. Hennekinne J-A, De Buyser M-L, Dragacci S (2012). Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev, 36 (4): 815-36.
20. Tamarapu S, McKILLIP JL, Drake M (2001). Development of a multiplex polymerase chain reaction assay for detection and differentiation of Staphylococcus aureus in dairy products. J Food Prot, 64 (5): 664-68.
21. Manders SM (1998). Toxin-mediated streptococcal and staphylococcal disease. J Am Acad Dermatol , 39 (3): 383-98.
22. Casaes Nunes RS, Pires de Souza C, Pereira KS et al (2016). Identification and molecular phylogeny of coagulase-negative staphylococci isolates from Minas Frescal cheese in southeastern Brazil: Superantigenic toxin production and antibiotic resistance. J Dairy Sci, 99 (4): 2641-53.
23. Chakravorty S, Helb D, Burday M et al (2007). A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods, 69 (2): 330-9.
24. Sami M NA, Bagheri M, Sharifi H (2013). Microbiological and chemical qualities of cream-filled pastries sold in Kerman city confectioneries, southeast of Iran. Eurasian J Vet Sci, 29 (3): 138-42.
25. Nikniaz Z MR, Jalilzadeh H, Vahed Jabbari M (2011). Evaluation of Microbial Contamination in Cream Filled Pastries Distributed in Tabriz Confectionaries. J Food Technol Nutr, 8 (1): 66-71.
26. Sharifzadeh A, Hajsharifi-Shahreza M, Ghasemi-Dehkordi P (2016). Evaluation of Microbial Contamination and Chemical Qualities of Cream-filled Pastries in Confectioneries of Chaharmahal Va Bakhtiari Province (Southwestern Iran). Osong Public Health Res Perspect, 7 (6): 346-350.
27. Zafarzadeh A, Mahfoozi A (2015). A Study on Staphylococcus aureus and Bacillus Cereus Contamination in Pastry Products in Gorgan. J Mazandaran Univ Med Sci, 25 (126): 143-47.
28. Omoe K, Ishikawa M, Shimoda Y et al (2002). Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harboring seg, seh, or sei genes. J Clin Microbiol, 40 (3): 857-62.
29. Kérouanton A, Hennekinne J, Letertre C et al (2007). Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol, 115 (3): 369-75.
30. Aydin A, Sudagidan M, Muratoglu K (2011). Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int J Food Microbiol, 148 (2): 99-106.
31. Yan X, Wang B, Tao X, Hu Q, et al (2012). Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China. Appl Environ Microbiol, 78 (18): 6637-42.
32. Gould IM, David MZ, Esposito S, et al (2012). New insights into meticillin-resistant Staphylococcus aureus (MRSA) pathogenesis, treatment and resistance. Int J Antimicrob Agents, 39 (2): 96-104.
33. Aydin A, Muratoglu K, Sudagidan M et al (2011). Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne Pathog Dis, 8 (1): 63-9.
34. Fontes CO, Silva VL, de Paiva MR et al (2013). Prevalence, antimicrobial resistance, and virulence characteristics of mecA-encoding coagulase-negative staphylococci isolated from soft cheese in Brazil. J Food Sci, 78 (4): M594-9.
2. Argudín MÁ, Mendoza MC, Rodicio MR (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel), 2 (7): 1751-73.
3. Ross S (2000). Functional foods: the Food and Drug Administration perspective. Am J Clin Nutr, 71 (6 Suppl): 1735S-38S.
4. Ameme DK, Abdulai M, Adjei EY et al (2016). Foodborne disease outbreak in a resource-limited setting: a tale of missed opportunities and implications for response. Pan Afr Med J, 23:69.
5. Karimi M, Nasr Esfahani B, Halaji M, et al (2017). Molecular characteristics and antibiotic resistance pattern of Staphylococcus aureus nasal carriage in tertiary care hospitals of Isfahan, Iran. Infez Med, 25: 234-240.
6. Schmitt M, Schuler-Schmid U, Schmidt-Lorenz W (1990). Temperature limits of growth, TNase and enterotoxin production of Staphylococcus aureus strains isolated from foods. Int J Food Microbiol, 11 (1): 1-19.
7. Sospedra I, Soriano JM, Mañes J (2013). Enterotoxinomics: The omic sciences in the study of staphylococcal toxins analyzed in food matrices. Food Res Int, 54 (1): 1052-60.
8. Pinchuk IV, Beswick EJ, Reyes VE (2010). Staphylococcal enterotoxins. Toxins (Basel), 2 (8): 2177-97.
9. Ortega E, Abriouel H, Lucas R, Gálvez A (2010). Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins (Basel), 2 (8): 2117-31.
10. Hoveida L, Ataei B, Amirmozafari N, Noormohammadi Z (2018). Species diversity and molecular analysis of Staphylococcus in confectioneries of a developing country, Iran. Infez Med, 26 (2): 148-54.
11. Standard A (2017). NCCLS document M38-A. National Committee for Clinical Laboratory Standards, Wayne, PA.
12. Rahdar HA, Azadi D, Shojaei H (2017). Molecular analysis and species diversity of Nocardia in hospital environment of a developing country, a potential health hazard. J Med Microbiol, 66 (3): 334-341.
13. Azadi D, Shojaei H, Pourchangiz M, et al (2016). Species diversity and molecular characterization of nontuberculous mycobacteria in hospital water system of a developing country, Iran. Microb Pathog, 100: 62-69.
14. Jeon Y-S, Chung H, Park S et al (2005). jPHYDIT: a JAVA-based integrated environment for molecular phylogeny of ribosomal RNA sequences. Bioinformatics, 21 (14): 3171-73.
15. McClure J-A, Conly JM, Lau V et al (2006). Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J Clin Microbiol, 44 (3): 1141-44.
16. Blaiotta G, Ercolini D, Pennacchia C, et al (2004). PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seI in S. aureus AB‐8802. J Appl Microbiol, 97 (4): 719-30.
17. Monday SR, Bohach GA (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol, 37 (10): 3411-14.
18. Dinges MM, Orwin PM, Schlievert PM (2000). Exotoxins of Staphylococcus aureus. Clin Microbiol Rev, 13 (1): 16-34.
19. Hennekinne J-A, De Buyser M-L, Dragacci S (2012). Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev, 36 (4): 815-36.
20. Tamarapu S, McKILLIP JL, Drake M (2001). Development of a multiplex polymerase chain reaction assay for detection and differentiation of Staphylococcus aureus in dairy products. J Food Prot, 64 (5): 664-68.
21. Manders SM (1998). Toxin-mediated streptococcal and staphylococcal disease. J Am Acad Dermatol , 39 (3): 383-98.
22. Casaes Nunes RS, Pires de Souza C, Pereira KS et al (2016). Identification and molecular phylogeny of coagulase-negative staphylococci isolates from Minas Frescal cheese in southeastern Brazil: Superantigenic toxin production and antibiotic resistance. J Dairy Sci, 99 (4): 2641-53.
23. Chakravorty S, Helb D, Burday M et al (2007). A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods, 69 (2): 330-9.
24. Sami M NA, Bagheri M, Sharifi H (2013). Microbiological and chemical qualities of cream-filled pastries sold in Kerman city confectioneries, southeast of Iran. Eurasian J Vet Sci, 29 (3): 138-42.
25. Nikniaz Z MR, Jalilzadeh H, Vahed Jabbari M (2011). Evaluation of Microbial Contamination in Cream Filled Pastries Distributed in Tabriz Confectionaries. J Food Technol Nutr, 8 (1): 66-71.
26. Sharifzadeh A, Hajsharifi-Shahreza M, Ghasemi-Dehkordi P (2016). Evaluation of Microbial Contamination and Chemical Qualities of Cream-filled Pastries in Confectioneries of Chaharmahal Va Bakhtiari Province (Southwestern Iran). Osong Public Health Res Perspect, 7 (6): 346-350.
27. Zafarzadeh A, Mahfoozi A (2015). A Study on Staphylococcus aureus and Bacillus Cereus Contamination in Pastry Products in Gorgan. J Mazandaran Univ Med Sci, 25 (126): 143-47.
28. Omoe K, Ishikawa M, Shimoda Y et al (2002). Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harboring seg, seh, or sei genes. J Clin Microbiol, 40 (3): 857-62.
29. Kérouanton A, Hennekinne J, Letertre C et al (2007). Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol, 115 (3): 369-75.
30. Aydin A, Sudagidan M, Muratoglu K (2011). Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int J Food Microbiol, 148 (2): 99-106.
31. Yan X, Wang B, Tao X, Hu Q, et al (2012). Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China. Appl Environ Microbiol, 78 (18): 6637-42.
32. Gould IM, David MZ, Esposito S, et al (2012). New insights into meticillin-resistant Staphylococcus aureus (MRSA) pathogenesis, treatment and resistance. Int J Antimicrob Agents, 39 (2): 96-104.
33. Aydin A, Muratoglu K, Sudagidan M et al (2011). Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne Pathog Dis, 8 (1): 63-9.
34. Fontes CO, Silva VL, de Paiva MR et al (2013). Prevalence, antimicrobial resistance, and virulence characteristics of mecA-encoding coagulase-negative staphylococci isolated from soft cheese in Brazil. J Food Sci, 78 (4): M594-9.
| Files | ||
| Issue | Vol 49 No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v49i1.3056 | |
| Keywords | ||
| Staphylococcal food poisoning Antibiotic resistance Sequence analysis Enterotoxins | ||
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How to Cite
1.
HOVEIDA L, ATAEI B, AMIRMOZAFARI N, NOORMOHAMMADI Z. Species Variety, Antibiotic Susceptibility Patterns and Prevalence of Enterotoxin Genes in Staphylococci Isolated from Foodstuff in Central Iran. Iran J Public Health. 2020;49(1):96-103.
