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Antimicrobial Resistance and Presence of Enterotoxins in Staphylococcus spp. Isolated from Cooked Meat and Desserts

Josi Guimarães César, Andriele Madruga Peres, Caroline Pereira das Neves, Marcos Roberto Alves Ferreira, Jozi Fagundes de Mello, Ângela Nunes Moreira, Kelly Lameiro Rodrigues
Journal of Food and Nutrition Research. 2017, 5(10), 750-753. DOI: 10.12691/jfnr-5-10-5
Published online: September 28, 2017

Abstract

The aim of this study was to isolate Staphylococcus spp. from cooked meat and desserts from restaurants and test for the presence of enterotoxins A, B, C, D, E genes and antimicrobial resistance profile. Thirty-six samples of cooked meat and thirty-six samples of desserts were collected from nine restaurants from Pelotas, Brazil. Staphylococcus spp. isolates were tested for antimicrobial susceptibility profile by disc diffusion method. Multiplex Polymerase Chain Reaction was performed to identify the presence of enterotoxins. Seven out of the 38 isolates registered the presence of any gene of traditional enterotoxins and enterotoxin E is the most frequent, with 42.8%, and five different genotypes were reported. Staphylococcus spp. isolates registered a high percentage of antimicrobial resistance to penicillin and oxacillin.

1. Introduction

People´s food habits are changing and have lunch outside the home has become a practical and fast alternative 1. However, meals may also disseminate pathogens which may be passed to food during processing, especially due to inadequate handling. And foodborne diseases (FB) may be a consequence of contamination, characterizing safe food as challenging 2.

Coagulase-positive Staphylococci (CoPS) is the pathogenic bacteria mainly associated to desserts and cooked meat, and have been extant for more than ten years among the most frequently identified FB agent in Brazil 3. CoPS may occur in food due to inadequate handling, and above high concentration (over 105 CFU/g), they may produce enterotoxins and cause FB outbreaks 4. The CoPs Staphylococcus aureus is the second most important pathogen involved in FB outbreaks in Brazil 3.

However, coagulase-negative Staphylococci (CoNS) are frequently isolated in food and may also produce enterotoxins 3, 5, 6. When food is insufficiently cooked, the proliferation of microorganism and the production of Staphylococcus enterotoxins (SEs) may occur. The enterotoxin (SE) genes are encoded in mobile genetic elements, such as plasmids, prophases and Staphylococcus pathogenic islands, and these mobile genetic elements are responsible for the horizontal transfer of virulence or antibiotic resistance genes between strains 7. Molecular analysis techniques are widely employed to identify and verify the expression of SE genes 8, and multiplex Polymerase Chain Reaction (mPCR) may be underscored for SEs analysis since it amplifies simultaneously several genes.

Besides that, Staphylococcus spp. may be resistant to several classes of antimicrobial agents and may cause numberless infections, and normally it is resistant to β-lactam antimicrobial agents, such as penicillin and oxacillin 9, 10. Staphylococcus infections have been on the increase during the last few years and, consequently, the number of multi-resistant strains, making difficult and prolonging the treatment of such infections 11, 12.

The aim of this study was isolate Staphylococcus spp. from cooked meat and desserts from restaurants and test for the presence of SE (A, B, C, D, E) genes and antimicrobial resistance profile.

2. Material and Methods

2.1. Isolation of Staphylococcus spp.

Thirty-six samples of cooked meat and 36 samples of desserts from restaurants of Pelotas city, Brazil were analyzed for the county of Staphylococcus spp. Samples were collected as if one was actually buying the ready food which was placed in disposable thermal packing, at the restaurant counter. The package was duly closed and taken to the Food Microbiology Laboratory at School of Nutrition at the Federal University of Pelotas for analysis.

For the isolation of Staphylococcus spp., samples were plated on Agar Baird Parker (BP, Merck®), enriched with egg yolk emulsion and potassium tellurite 1% by surface spreading, and incubated at 37°C for 48h. Further, presumed typical and atypical colonies were counted and given as Colony-Forming Units per gram of food (CFU/g). Three typical and three atypical colonies were isolated and Gram-stained e confirmed colonies were tested for coagulase 13.

2.2. Resistance to Antimicrobial Factors

Staphylococcus spp. isolates were verified for resistance to antimicrobial agents by the disc diffusion technique, as recommended by the Clinical and Laboratory Standards Institute 14. The isolates were first streaked in BHI broth (Merck®) at 36°C and inoculated in a saline solution 0.85% (Merck®) till 0.5 of Mac Farland scale. The culture was then spread on plates with Muller Hinton Agar (MH, Merck®) where the discs of antimicrobial agents for Gram-positive bacteria (Invitrogen®) were placed and incubated at 37°C for 24h. Zone of inhibition were measured and compared by CLSI resistance standard table 14. The tested twelve antimicrobial agents that formed the antimicrobial disc were ampicillin (10µg), penicillin (10 units), oxacillin (1µg), clindamycin (2µg), sulfamethoxazole/trimethoprim (23.75/1.25µg), chloramphenicol (30µg), erythromycin (15µg), gentamicin (10µg), tetracycline (30µg), vancomycin (30µg), ciprofloxacin (5µg), cefepime (30µg) and rifampicin (5µg).

2.3. Verification of Enterotoxins Staphylococcus Genes

DNA chromosome was extracted from Staphylococcus spp. isolates with commercial kit (PureLink Genomic DNA – K1820-01, Invitrogen®). Extracted DNA underwent mPCR technique to verify the presence of SEs A, B, C, D and E genes. Primers to identify SEs genes were described by Mehrotra et al. 15 (Table 1).

Moreover, 1μl of each primer GSEAR-1/ GSEAR-2, GSECR-1/ GSECR-2, GSEDR-1/ GSEDR-2 was used in the first mPCR block; 2.5μl buffer solution for PCR (10x); 1.5μl magnesium chloride (MgCl2) (5U/μl); 0.5μl of mix dNTPs (100nM), 0.3μl of Taq DNA polymerase (500U) and 1μl of DNA in 25μl of final volume. The second reaction block comprised the same reagents but primers were GSEBR-1/ GSEBR-2, GSEER-1/ GSEER-2. Further, mPCRs were done in thermal cycler (MJ Research, PTC-100, Peltier Thermal Cycler) at the following conditions: 95°C for 5min; 30 cycles (95°C – 30’’; 55°C – 1’ and 72°C – 1’) and final extension at 72°C for 7min.

All mPCR products were analyzed by agar gel electrophorese 1.5% (Invitrogen) stained with ethyl bromide (Promega®), seen without transluminator, and photographed (Kodak Digital Science TM DC120). A 100pb DNA Ladder (Ludwig Biotec®) was the molecular mass marker. Negative control of reactions had the same compositions as mPCR, although sterile Milli-Q-waterreplaced DNA. DNAs of S. aureus ATCCs 13565 (EEA), 14458 (EEB), 19095 (EEC), 23235 (EED) and 21664 (EEE) were used as positive controls.

3. Results and discussion

Table 2 shows results for the quantification of Staphylococcus spp. in cooked meat samples and dessert samples.

Of the seventy-two samples of cooked meat and desserts, five (6.9%) were contaminated with CoPS, but within standard limits permitted by Brazilian sanitary law, up to 103 CFU/g 16, and CoNS counts were isolated in 33 samples (45.8%).

A study in Porto Alegre, Brazil evaluated 26 samples from several types of food, which included cooked meat and desserts, and reported 15 samples contaminated with CoNS and none with CoPS. 17 Other study evaluated 82 samples of desserts from university cafeterias in Greece, with 76.8% (n=63) of samples contaminated by Staphylococcus spp. 18.

Brazilian sanitary law only concentrates on the investigation of CoPS in food due to their pathogenicity 16, but CoNS may also produce enterotoxins. Seven out of the 38 isolates registered the presence of any gene of traditional SEs and SEE is the most frequent, with 42.8%. Five different genotypes were reported (Table 3).

Moreover, 85.7% of the 7 positive isolates of SE genes were CoNS. Only one of the five CoPS isolates, from a dessert sample, had SE genes (SE E). SEE is not the most frequent SE in food or in outbreaks 19, 20. Xing et al. 21 evaluated 128 S. aureus isolates from ready-to-eat food and reported SED in 28.5% of food, whereas SEE represented only 2.3% (n=3). Mello et al. 17 evaluated isolates of Staphyloccocus spp. in 26 samples of ready-to-eat food and registered SEB in 42.1% and SE only associated with another SE (SEB and SED).

SEA seems to be the most frequent gene in food and the most common in food Staphylococcus intoxication. However, SE E gene has already been registered in food intoxication 4, 22. Ostyn et al. 23 reported the first food intoxication by SEE in France due to common cheese made from non-pasteurized milk. Cheese analysis registered S. aureus counts of < 10² UFC/g and quantification of 0.45 ng of SEE. SEE is 79 – 90% structurally similar to SEA and may be potentially pathogenic. Further, the thermo-stability of SE provides selective resistance 24. Consequently, processes in food production that reduce vegetative cells are effective for food safety.

All Staphylococcus spp. isolates (n=38) were tested for antimicrobial resistance. They are greatly resistant to penicillin (39.5%) and oxacillin (34.2%), intermediate resistance to erythromycin (5.3%) and rifampicin (2.6%). Further, all isolates were sensitive to the antimicrobial agents chloramphenicol, gentamicin, tetracycline and sulfamethoxazole/trimethoprim and 5.3% (n=2) of isolates were multi-resistant (Table 4).

Further, 68.7% and 66.6% of Staphylococcus spp. isolates respectively from meat (n=16) and dessert (n=22) were resistant to at least one antimicrobial agent. Only 12% (n=25) of all isolates resistant to any antimicrobial agent were CoPS. One isolate from a dessert (CoNS) was resistant to six antimicrobial agents (clindamycin, vancomycin, erythromycin, chloramphenicol, rifampicin, cefepime, oxacillin and penicillin).

Similar studies evaluating the antimicrobial resistance of Staphylococcus spp. isolates registered 53.8% (n=80) which were resistant to penicillin 25; 23.1% (n=78) to oxacillin 26 and approximately 100% (n=16) sensitive to chloramphenicol, gentamycin, tetracycline and sulfamethoxazole/trimethoprim 27 Penicillin and oxacillin intervene in the synthesis and remodeling of bacterial peptidoglycans. Penicillin-binding proteins (PBPs) have a low affinity for antimicrobial agents. When they replace other PBPs, the survival of bacteria occurs in high concentrations. Although penicillin was the first antibiotic to combat S. aureus-caused infections, its excessive and inadequate use favored the bacterium’s resistance capacity to the antimicrobial agents 26, 28, 29.

4. Conclusion

Staphylococcus spp. isolates registered a high percentage of antimicrobial resistance to penicillin and oxacillin. SE E gene was the most frequent among Staphylococcus spp. isolates. Results demonstrate the importance of quality procedures in food production because they control important pathogens and, consequently, the enterotoxins in food, mainly in eat-to-eat products produced by restaurants.

Acknowledgements

The researchers would like to thank the financial support from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brasilia, Brazil).

References

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In article      PubMed  PubMed
 
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Published with license by Science and Education Publishing, Copyright © 2017 Josi Guimarães César, Andriele Madruga Peres, Caroline Pereira das Neves, Marcos Roberto Alves Ferreira, Jozi Fagundes de Mello, Ângela Nunes Moreira and Kelly Lameiro Rodrigues

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Cite this article:

Normal Style
Josi Guimarães César, Andriele Madruga Peres, Caroline Pereira das Neves, Marcos Roberto Alves Ferreira, Jozi Fagundes de Mello, Ângela Nunes Moreira, Kelly Lameiro Rodrigues. Antimicrobial Resistance and Presence of Enterotoxins in Staphylococcus spp. Isolated from Cooked Meat and Desserts. Journal of Food and Nutrition Research. Vol. 5, No. 10, 2017, pp 750-753. http://pubs.sciepub.com/jfnr/5/10/5
MLA Style
César, Josi Guimarães, et al. "Antimicrobial Resistance and Presence of Enterotoxins in Staphylococcus spp. Isolated from Cooked Meat and Desserts." Journal of Food and Nutrition Research 5.10 (2017): 750-753.
APA Style
César, J. G. , Peres, A. M. , Neves, C. P. D. , Ferreira, M. R. A. , Mello, J. F. D. , Moreira, Â. N. , & Rodrigues, K. L. (2017). Antimicrobial Resistance and Presence of Enterotoxins in Staphylococcus spp. Isolated from Cooked Meat and Desserts. Journal of Food and Nutrition Research, 5(10), 750-753.
Chicago Style
César, Josi Guimarães, Andriele Madruga Peres, Caroline Pereira das Neves, Marcos Roberto Alves Ferreira, Jozi Fagundes de Mello, Ângela Nunes Moreira, and Kelly Lameiro Rodrigues. "Antimicrobial Resistance and Presence of Enterotoxins in Staphylococcus spp. Isolated from Cooked Meat and Desserts." Journal of Food and Nutrition Research 5, no. 10 (2017): 750-753.
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  • Table 3. Genotype of Staphylococcus spp. isolates from food with regard gene of traditional enterotoxins
  • Table 4. Results of resistance test to antimicrobial agents of Staphylococcus spp. isolated from cooked meat and desserts
[1]  Pereira, E.L., Rodrigues, A. and Ramalhosa, E, “Influence of working conditions and practices on fresh-cut lettuce salads quality” Food Control, 33 (2). 406-412. 2013.
In article      View Article
 
[2]  Cambero, M.I., Cabeza, M.C., Escudero, R., Manzano, S., Garcia-Márquez, I., Velasco, R. and Ordóñez, J.A, “Sanitation of selected ready-to-eat intermediate-moisture foods of animal origin by e-beam irradiation” Foodborne Pathogen Disease, 9 (7). 594-599. 2012.
In article      View Article  PubMed
 
[3]  Brasil. “Vigilância Epidemiológica das Doenças de Transmissão de Alimentos Hídrica e Alimentar. Dados epidemiológicos - DTA período de 2010 a 2014”, 2014 [Online]. Available: http://www.anrbrasil.org.br/new/pdfs/2014/3_PAINEL_1_ApresentacaoRejaneAlvesVigilanciaEpidemiologica-VE-DTA-Agosto_2014_PDF.pdf 2015 [Acessed Feb. 16, 2016].
In article      View Article
 
[4]  Kadariya, J., Smith, T.C. and Thapaliya, D, “Staphylococcus aureus and Staphylococcal Food-Borne Disease: An Ongoing Challenge in Public Health” BioMed Research International, 1-9. 2014.
In article      View Article  PubMed
 
[5]  Lyra, D.G., Sousa, F.G., Borges, M.F., Givisiez, P.E., Queiroga, R.C., Souza, E.L. and Oliveira, C.J.B, “Enterotoxin-Encoding Genes in Staphylococcus spp. from Bulk Goat Milk” Foodborne Pathogen and Disease, 10 (2). 126-130. 2013.
In article      View Article  PubMed
 
[6]  Rall, V.L., Miranda, E.S., Castilho, I.G., Camargo, C.H., Langoni, H., Guimarães, F.F., Araujo Junior, J.P. and Fernandes Junior, A, “Diversity of Staphylococcus species and prevalence of enterotoxin genes isolated from milk of healthy cows and cows with subclinical mastitis” Journal of Dairy Science, 97 (2). 829-837. 2014.
In article      View Article  PubMed
 
[7]  Maiques, E., Ubeda, C., Campoy, S., Salvador, N., Lasa, I., Novick, R.P., Barbe, J. and Penades, J.R, “B-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus” Journal of Bacteriology, 1188. 2726-2729. 2006.
In article      View Article  PubMed
 
[8]  Pelisser, M.R., Klein, C.S., Ascoli, K.R., Zotti, T.R. and Arisi, A.M, “Ocurrence of Staphylococcus aureus and multiplex PCR detection of classic enterotoxin genes in cheese and meat products” Brazilian Journal of Microbiology, 40. 145-148. 2009.
In article      View Article  PubMed
 
[9]  Rizek, C.F., Matté, M.H., Dropa, M., Mamizuka, E.M., Almeida, L.M., Lincopan, N., Matté, G.R. and Germano, P.M, “Identification of Staphylococcus aureus carrying the mecA gene in ready-to-eat food products sold in Brazil” Foodborne Pathogen Disease, 8 (4). 561-563. 2011.
In article      View Article  PubMed
 
[10]  Regecová, I., Pipová, M., Jevinová, P., Marušková, K., Kmeť, V. and Popelka, P, “Species Identification and Antimicrobial Resistance of Coagulase-Negative Staphylococci Isolated from the Meat of Sea Fish” Journal of Food Science, 79 (5). 898-902. 2014.
In article      View Article  PubMed
 
[11]  Montoya, I.C., Mira, M.O., Álvarez, I.A., Cofre, J.G., Cohen, J.V., Donoso, G.W. and Torrest, J.P, “Resistencia inducible a clindamicina em Staphylococcus aureus meticilino resistente” Revista Chilena de Pediatria. 80 (1). 48-53. 2009.
In article      View Article
 
[12]  Rinsky, J.L., Nadimpalli, M., Wing, S., Hall, D., Baron, D., Price, L.B., Larsen, J., Stegger, M., Stewart, J. and Christopher, H.D, “Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in North Carolina” PLoS One, 8 (7). 2013.
In article      View Article  PubMed
 
[13]  Food and Drug Administration, “Bacteriological Analytical Manual”, 2001 [Online]. Available: http://911emg.com/Ref%20Library%20ERG/FDA%20Bacteriological%20Analysis.pdf [Acessed Feb. 3, 2016].
In article      View Article
 
[14]  Clinical and Laboratory Standards Institute. “Performance standard for antimicrobial susceptibility testing”, 2007 [Online]. Available: http://www.microbiolab-bg.com/CLSI.pdf [Acessed Feb. 3, 2016].
In article      View Article
 
[15]  Mehrotra, M., Wang, G. and Johnson, W.M, “Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance” Journal of Clinical Microbiology, 38 (3). 1032-1035. 2000.
In article      PubMed  PubMed
 
[16]  Brasil. “Regulamento Técnico sobre padrões microbiológicos para alimentos. Resolução RDC nº 12, January 02, 20012, 2001 [Online]. Available: http://portal.anvisa.gov.br/wps/wcm/connect/a47bab8047458b909541d53fbc4c6735/RDC_12_2001.pdf?MOD=AJPERES [Acessed Feb. 3, 2016].
In article      View Article
 
[17]  Mello, J.F., Rocha, L.B., Lopes, E.S., Frazzon, J. and Costa, M, “Sanitary quality, occurrence and identification of Staphylococcus sp. in food services” Brazilian Journal of Microbiology, 45 (3). 1031-1037. 2014.
In article      View Article  PubMed
 
[18]  Kotzekidou, P, “Microbiological examination of ready-to-eat foods and ready-to-bake frozen pastries from university canteens” Food Microbiology, 34 (2). 337-343. 2013.
In article      View Article  PubMed
 
[19]  Argudín, M.A., Mendoza, M.C. and Rodicio, M.R, “Food Poisoning and Staphylococcus aureus Enterotoxins” Toxins (Basel) 2 (7). 1751-1773. 2010.
In article      View Article  PubMed
 
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