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Prevalence and characterization of methicillin susceptible Staphylococcus aureus ST398 isolates from retail foods

https://doi.org/10.1016/j.ijfoodmicro.2014.12.002Get rights and content

Highlights

  • The first comprehensive study on S. aureus ST398 isolated from foods in China.

  • Low prevalence of MSSA ST398 in food.

  • S. aureus ST398 harbored multiple resistance and virulence genes.

  • S. aureus ST398 exhibited a multi-resistance phenotype.

  • Features of ST398 overlapped with those causing human and animal infections.

Abstract

In this study, we explored the prevalence of Staphylococcus aureus (S. aureus) ST398 in retail foods and then investigated for their virulence and antimicrobial resistance genetic background. Fourteen out of 5103 (0.27%) samples were positive for methicillin susceptible S. aureus (MSSA) ST398. Resistance was most frequently observed to penicillin (PEN) (100%), followed by trimethoprim (TMP), erythromycin (ERY) and ampicillin (AMP) (each 86.7%), clindamycin (CLD, 80.0%), and tetracycline (TET, 26.7%). All ST398 isolates were susceptible to amikacin, chloramphenicol, cefoxitin, gentamicin, oxacillin, and vancomycin. Two predominant resistance patterns including TMP-ERY-CLD-PEN-AMP (60.0%) and TMP-ERY-TET-CLD-PEN-AMP (20.0%) were identified. Isolates harbored blaZ (86.7%) gene, followed by tet(L) and linA/linA′ (each 46.7%), ermB and msrA (each 33.3%), aph(3′)-IIIa and dfrK (each 26.7%), tet(K) (20.0%), ant(4′)-Ia, ermA and emrC (each 13.3%) and cat::pC221 (6.7%). No isolate carried mecA, tet(M), tet(O), fexA, aac(6′)/aph(2″), cfr, ermT, msrB, cat::pC194, cat::pC223, catpIp-501, dfrD, dfrG and dfrS1 genes. For virulence genes, hld (73.3%), seb and sed (each 66.7%), hla (60.0%), lukPV (33.3%), sej (26.7%), lukED and seg (each 3.3%) were detected. None of isolates contained sea, sec, see, seh, sei, tst, eta, etb, sek-ser, seu, lukM, hlg, and hlgv genes. Four spa types were found, including t571 (6/15), t034 (4/15), t2876 (3/15) and t1250 (2/15). All strains were non-typeable for agr locus. Our findings indicated that MSSA ST398 isolates had a low prevalence rate in retail foods, and these isolates harbored multiple virulence and antimicrobial resistance genes, and exhibited multiple antimicrobial resistance. Further studies are required to elucidate the possible role of MSSA ST398 as a source of human infection.

Introduction

Methicillin-resistant and -susceptible Staphylococcus aureus (S. aureus) (MRSA and MSSA) sequence type 398 (ST398) can colonize animals and humans and be transmitted between them (Jamrozy et al., 2012, Mediavilla et al., 2012, Yan et al., 2014). S. aureus ST398 strains are non-typeable by standard SmaI pulsed-field gel electrophoresis (PFGE) analysis due to DNA methylation. It is reported that MRSA ST398 strains are usually found in pigs and workers on pig farms in many countries (Argudin et al., 2011, Huber et al., 2010, Lozano et al., 2009, Verhegghe et al., 2013). MRSA ST398 isolates exhibited multidrug resistance (MDR) phenotypes to beta-lactam antibiotics as well as non-β-lactam antimicrobial agents (Verhegghe et al., 2013), which represented a risk to human health. However, due to a lack of staphylococcal cassette chromosome mec (SCCmec) gene, MSSA ST398 was susceptible to a part of β-lactam antimicrobials (Mediavilla et al., 2012, Yan et al., 2014). Recently, infections caused by MSSA ST398 have been described in humans (David et al., 2013, Mediavilla et al., 2012, Valentin-Domelier et al., 2011), and MSSA ST398 seems to be more frequent to cause infections than those caused by MRSA ST398.

Although the presence of MRSA ST398 in retail meat products (Argudin et al., 2011, Lozano et al., 2009) and MSSA ST398 in pigs (Yan et al., 2014) has been extensively studied, the characteristics of MSSA ST398 isolates collected from retail foods in China have not been fully explored. Therefore, the aim of this study was to characterize these MSSA ST398 strains by determining antimicrobial susceptibility, resistance and toxin genes.

Section snippets

Bacterial strains

A total of 5103 food samples including 490 ready-to-eat foods, 1392 raw chicken, 160 pork, 120 dumplings, 1069 bovine raw milk samples, 910 goat milk powder processing samples, 245 powdered infant formula, 447 infant rice cereals and 270 raw egg samples were collected at different times during the period of July 2008 to March 2014. Isolation and identification of S. aureus (1–2 isolates per sample) were performed as described previously by Wang et al. (2014). All isolates were analyzed by PFGE

Prevalence of S. aureus ST398

Table 1 lists the prevalence of S. aureus ST398 strains in the 5103 food samples examined. We recovered 1428 S. aureus isolates (1–2 isolates per sample) including 1413 typeable strains and 15 non-typeable strains by standard SmaI PFGE. Fifteen non-typeable strains were confirmed as S. aureus ST398 by MLST. A total of 14 samples were positive for S. aureus ST398, including 2 ready-to-eat foods, 5 raw chickens, 4 raw cow milk and 3 raw goat milk. All S. aureus ST398 isolates were negative for mecA

Discussion

Previous studies indicated that MRSA ST398 has been detected in various animal-borne food products (Argudin et al., 2011, Lozano et al., 2009). However, no comprehensive study has been performed on the prevalence of MSSA ST398 in retail foods. MSSA ST398 was detected at a low rate (0.27%) in retail foods in this study. No MRSA ST398 was detected, which contrasts with other studies reporting MRSA ST398 in meat (Argudin et al., 2011, Lozano et al., 2009). While the real pathogenicity of MSSA

Acknowledgments

This research was in supported by the National Natural Science Foundation of China (No. 31271858), the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (2012BAK01B02) and the Special Fund for Agro-scientific Research in the Public Interest (201203040).

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