Occurrence, Antibiotic Susceptibility, Biofilm Formation and Molecular Characterization of Staphylococcus aureus Isolated from Raw Shrimp in China

The aim of this study was to determine the prevalence and characterization of Staphylococcus aureus isolated from 145 shrimp samples from 39 cities in China. The results show that 41 samples (28%) from 24 cities were positive, and most of the positive samples (39/41, 95.1%) were less than 110 MPN/g. Antimicrobial susceptibility testing showed that only seven isolates were susceptible to all 24 antibiotics, whereas 65.1% were multidrug-resistant. Antibiotic resistance genes that confer resistance to β-lactams, aminoglycosides, tetracycline, macrolides, lincosamides and streptogramin B (MLSB), trimethoprim, fosfomycin and streptothricin antibiotics were detected. All S. aureus isolates had the ability to produce biofilm and harbored most of the biofilm-related genes. Genes encoding one or more of the important virulence factors staphylococcal enterotoxins (sea, seb and sec), toxic shock syndrome toxin 1 (tsst-1) and Panton–Valentine leukocidin (PVL) were detected in 47.6% (30/63) of the S. aureus isolates. Molecular typing showed that ST15-t085 (27.0%, 17/63), ST1-t127 (14.3%, 9/63) and ST188-t189 (11.1%, 7/63) were the dominant genetic types. The finding of this study provides the first comprehensive surveillance on the incidence of S. aureus in raw shrimp in China. Some retained genotypes found in this food have been linked to human infections around the world.

[1]  W. Gao,et al.  Molecular Characteristics of Staphylococcus aureus From Food Samples and Food Poisoning Outbreaks in Shijiazhuang, China , 2021, Frontiers in Microbiology.

[2]  V. Fusco,et al.  Novel insights into the enterotoxigenic potential and genomic background of Staphylococcus aureus isolated from raw milk. , 2020, Food microbiology.

[3]  P. Speziale,et al.  The Multivalent Role of Fibronectin-Binding Proteins A and B (FnBPA and FnBPB) of Staphylococcus aureus in Host Infections , 2020, Frontiers in Microbiology.

[4]  H. B. Tokman,et al.  Presence of Biofilm and Adhesin Genes in Staphylococcus aureus Strains Taken from Chronic Wound Infections and their Genotypic and Phenotypic Antimicrobial Sensitivity Patterns. , 2020, Photodiagnosis and photodynamic therapy.

[5]  Juan Wang,et al.  Phenotypic and genotypic characterization of PVL-positive Staphylococcus aureus isolated from retail foods in China. , 2019, International journal of food microbiology.

[6]  Juan Wang,et al.  Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China , 2019, Frontiers in Microbiology.

[7]  Yanmei Huang,et al.  Prevalence and Characterization of Staphylococcus aureus Isolated From Women and Children in Guangzhou, China , 2018, Front. Microbiol..

[8]  Juan Wang,et al.  Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity , 2018, Front. Microbiol..

[9]  Chentao Yang,et al.  The Changing Pattern of Population Structure of Staphylococcus aureus from Bacteremia in China from 2013 to 2016: ST239-030-MRSA Replaced by ST59-t437 , 2018, Front. Microbiol..

[10]  N. Botteldoorn,et al.  Food-Borne Outbreak Investigation and Molecular Typing: High Diversity of Staphylococcus aureus Strains and Importance of Toxin Detection , 2017, Toxins.

[11]  S. Fanning,et al.  Enterotoxigenicity and Antimicrobial Resistance of Staphylococcus aureus Isolated from Retail Food in China , 2017, Front. Microbiol..

[12]  Mingfang Xu,et al.  Prevalence, Virulence Genes, Antimicrobial Susceptibility, and Genetic Diversity of Staphylococcus aureus from Retail Aquatic Products in China , 2017, Front. Microbiol..

[13]  G. La Salandra,et al.  Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. , 2017, Food microbiology.

[14]  S. Gill,et al.  Adaptive Upregulation of Clumping Factor A (ClfA) by Staphylococcus aureus in the Obese, Type 2 Diabetic Host Mediates Increased Virulence , 2017, Infection and Immunity.

[15]  S. Correa,et al.  Evaluation of the biofilm forming ability and its associated genes in Staphylococcus species isolates from bovine mastitis in Argentinean dairy farms. , 2017, Microbial pathogenesis.

[16]  E. Owusu-Dabo,et al.  Nasal Carriage of Staphylococcus aureus among Children in the Ashanti Region of Ghana , 2017, PloS one.

[17]  Á. Soriano,et al.  Methicillin-resistant Staphylococcus aureus infections: A review of the currently available treatment options. , 2016, Journal of global antimicrobial resistance.

[18]  Raymond Lo,et al.  CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database , 2016, Nucleic Acids Res..

[19]  S. Khoramrooz,et al.  Detection of biofilm related genes, classical enterotoxin genes and agr typing among Staphylococcus aureus isolated from bovine with subclinical mastitis in southwest of Iran. , 2016, Microbial pathogenesis.

[20]  A. Beaussart,et al.  Sticky Matrix: Adhesion Mechanism of the Staphylococcal Polysaccharide Intercellular Adhesin. , 2016, ACS nano.

[21]  G. Spano,et al.  Molecular characterization of Staphylococcus aureus isolated from sheep and goat cheeses in southern Italy , 2016 .

[22]  Jian Yang,et al.  VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on , 2015, Nucleic Acids Res..

[23]  E. Zanardi,et al.  Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity , 2015 .

[24]  Kok-Gan Chan,et al.  Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shrimps in Malaysia , 2015, Front. Microbiol..

[25]  H. Hizlisoy,et al.  Occurence and antimicrobial resistance of Staphylococcus aureus and Salmonella spp. in retail fish samples in Turkey. , 2015, Marine pollution bulletin.

[26]  P. Worning,et al.  Comparing Whole-Genome Sequencing with Sanger Sequencing for spa Typing of Methicillin-Resistant Staphylococcus aureus , 2014, Journal of Clinical Microbiology.

[27]  A. Fetsch,et al.  Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. , 2014, International journal of food microbiology.

[28]  Wilmara Salgado-Pabón,et al.  Staphylococcal toxic shock syndrome: superantigen-mediated enhancement of endotoxin shock and adaptive immune suppression , 2014, Immunologic Research.

[29]  K. Demnerova,et al.  Staphylococcus aureus mobile genetic elements , 2014, Molecular Biology Reports.

[30]  Timothy J. Foster,et al.  Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus , 2013, Nature Reviews Microbiology.

[31]  S. Darwish,et al.  Investigation of Biofilm Forming Ability in Staphylococci Causing Bovine Mastitis Using Phenotypic and Genotypic Assays , 2013, TheScientificWorldJournal.

[32]  J. Bray,et al.  MLST revisited: the gene-by-gene approach to bacterial genomics , 2013, Nature Reviews Microbiology.

[33]  C. Torres,et al.  Detection of Methicillin-Susceptible Staphylococcus aureus ST398 and ST133 Strains in Gut Microbiota of Healthy Humans in Spain , 2013, Microbial Ecology.

[34]  Anne M Johnson,et al.  The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis , 2013, The Lancet. Infectious diseases.

[35]  H. Grundmann,et al.  Characterization of Staphylococcus aureus Strains Associated with Food Poisoning in Shenzhen, China , 2012, Applied and Environmental Microbiology.

[36]  S. Rasmussen,et al.  Identification of acquired antimicrobial resistance genes , 2012, The Journal of antimicrobial chemotherapy.

[37]  Sylviane Dragacci,et al.  Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. , 2012, FEMS microbiology reviews.

[38]  S. Virdis,et al.  Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese. , 2012, International journal of food microbiology.

[39]  H. Purohit,et al.  Molecular characterization of intercellular adhesion gene in Staphylococcus aureus isolated from bovine mastitic milk , 2012, Tropical Animal Health and Production.

[40]  I. Beleneva Incidence and characteristics of Staphylococcus aureus and Listeria monocytogenes from the Japan and South China seas. , 2011, Marine pollution bulletin.

[41]  M. Argudín,et al.  Food Poisoning and Staphylococcus aureus Enterotoxins , 2010, Toxins.

[42]  R. Daum,et al.  Community-Associated Methicillin-Resistant Staphylococcus aureus: Epidemiology and Clinical Consequences of an Emerging Epidemic , 2010, Clinical Microbiology Reviews.

[43]  H. Deeth,et al.  Prevalence, persistence and control of Salmonella and Listeria in shrimp and shrimp products: A review , 2010 .

[44]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[45]  F. Lowy Staphylococcus aureus infections. , 2009, The New England journal of medicine.

[46]  P. Gibbs,et al.  Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. , 2009, Food microbiology.

[47]  L. Su,et al.  Comparative molecular analysis of community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus isolates from children in northern Taiwan. , 2008, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[48]  F. B. Abdallah,et al.  Detection by PCR of adhesins genes and slime production in clinical Staphylococcus aureus , 2008, Journal of basic microbiology.

[49]  S. Simon,et al.  Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers , 2007 .

[50]  G. Normanno,et al.  Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. , 2007, International journal of food microbiology.

[51]  Y. Park,et al.  Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea , 2006, Journal of applied microbiology.

[52]  K. Omoe,et al.  An outbreak of staphylococcal food poisoning caused by enterotoxin H in mashed potato made with raw milk. , 2005, FEMS microbiology letters.

[53]  S. Scuota,et al.  Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. , 2005, International journal of food microbiology.

[54]  J. Takahashi,et al.  Pomegranate extract inhibits Staphylococcus aureus growth and subsequent enterotoxin production. , 2005, Journal of ethnopharmacology.

[55]  F. Hamadi,et al.  Effect of pH on distribution and adhesion of Staphylococcus aureus to glass , 2005 .

[56]  John-hwa Lee Methicillin (Oxacillin)-Resistant Staphylococcus aureus Strains Isolated from Major Food Animals and Their Potential Transmission to Humans , 2003, Applied and Environmental Microbiology.

[57]  M. Enright The evolution of a resistant pathogen--the case of MRSA. , 2003, Current opinion in pharmacology.

[58]  K. Venkitanarayanan,et al.  Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. , 2003, Veterinary microbiology.

[59]  P. Vanhems,et al.  Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients , 2002, The Lancet.

[60]  J. McLauchlin,et al.  The detection of enterotoxins and toxic shock syndrome toxin genes in Staphylococcus aureus by polymerase chain reaction. , 2000, Journal of food protection.

[61]  J. Holah,et al.  Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms , 1999, Journal of applied microbiology.

[62]  L. S. Carmo,et al.  Enterotoxin H in Staphylococcal Food Poisoning. , 1996, Journal of food protection.

[63]  Y. Su,et al.  Detection of staphylococcal enterotoxin H by an enzyme-linked immunosorbent assay. , 1996, Journal of food protection.

[64]  P. François,et al.  Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin‐binding proteins and studies on the expression of fnb genes , 1995, Molecular microbiology.

[65]  P. François,et al.  Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts , 1995, Infection and immunity.

[66]  D. Pittet,et al.  Fibronectin is more active than fibrin or fibrinogen in promoting Staphylococcus aureus adherence to inserted intravascular catheters. , 1993, The Journal of infectious diseases.

[67]  E. Igbinosa,et al.  Characterization of enterotoxigenic Staphylococcus aureus from ready-to-eat seafood (RTES) , 2021 .

[68]  B. Kreiswirth,et al.  The tst gene associated Staphylococcus aureus pathogenicity island facilitates its pathogenesis by promoting the secretion of inflammatory cytokines and inducing immune suppression. , 2019, Microbial pathogenesis.

[69]  A. Mirshafiey,et al.  Study of the Prevalence of Staphylococcus Aureus in Marine and Farmed Shrimps in Iran Aiming the Future Development of a Prophylactic Vaccine , 2015 .

[70]  Xin Wang,et al.  Staphylococcus aureus ST6-t701 isolates from food-poisoning outbreaks (2006-2013) in Xi'an, China. , 2015, Foodborne pathogens and disease.

[71]  K. Biao Identification of Staphylococcus aureus and SpA polymorphisms in Ma'anshan City , 2011 .

[72]  S. Barbuddhe,et al.  Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis , 2009, Veterinary Research Communications.

[73]  H. Rohde,et al.  Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. , 2007, Biomaterials.

[74]  W. Schaffner,et al.  An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. , 2002, Emerging infectious diseases.

[75]  A. Rasooly,et al.  Staphylococcal enterotoxins. , 2000, International journal of food microbiology.