Skip to main content
Top
Published in: World Journal of Pediatrics 2/2021

01-04-2021 | Staphylococcal Scalded Skin Syndrome | Original Article

Clinical and molecular characteristics of Staphylococcus aureus isolated from Chinese children: association among the agr groups and genotypes, virulence genes and disease types

Authors: Yan Xu, Su-Yun Qian, Kai-Hu Yao, Fang Dong, Wen-Qi Song, Chen Sun, Xin Yang, Jing- Hui Zhen, Xi-Qing Liu, Zhi -Yong Lv, Xi Yang

Published in: World Journal of Pediatrics | Issue 2/2021

Login to get access

Abstract

Background

This study was aimed to investigate the clinical and molecular epidemiology of Staphylococcus aureus (S. aureus) isolated from Chinese children and determine the possible relationship among the accessory gene regulator (agr) groups and genotypes, as well as among the virulence genes and disease types.

Methods

S. aureus strains were isolated from Beijing Children’s Hospital between October 2017 and October 2019. The isolates and 19 virulence genes were characterized using multi-locus sequence typing, staphylococcal protein A (spa), staphylococcal cassette chromosome mec, and agr typing.

Results

A total of 191 non-repetitive S. aureus clinical isolates were divided into 33 sequence types (STs), 18 clonal complexes (CCs), and 59 spa types. ST59 (39.8%), t437 (37.7%), and agr I (84.8%) were the predominant types. CC59, CC25, CC22, CC951, CC8, and CC398 belonged to agr I. CC5 and CC15 were assigned to agr II, and CC30 was characterized as agr III. CC121 was classified under agr IV. The eta, etb, and bbp genes were more prevalent in agr IV (P < 0.001 for each), while tst was more prevalent in agr group III compared to the other groups (P < 0.001). Nearly all isolates that harbored lukS/F-PV belonged to agr I (P = 0.005). However, the correlation between disease types and agr groups was not significant (P > 0.05).

Conclusions

An association among the agr groups and genotypes, as well as specific toxin genes, was observed among the S. aureus strains isolated from Chinese children. However, a statistical correlation was not found among the agr groups and disease types.
Appendix
Available only for authorised users
Literature
2.
go back to reference Liu Y, Xu Z, Yang Z, Sun J, Ma L. Characterization of community-associated Staphylococcus aureus from skin and soft-tissue infections: a multicenter study in China. Emerg Microbes Infect. 2016;5:e127.PubMedPubMedCentral Liu Y, Xu Z, Yang Z, Sun J, Ma L. Characterization of community-associated Staphylococcus aureus from skin and soft-tissue infections: a multicenter study in China. Emerg Microbes Infect. 2016;5:e127.PubMedPubMedCentral
3.
go back to reference Hu F, Zhu D, Wang F, Wang M. Current status and trends of antibacterial resistance in China. Clin Infect Dis. 2018;67(Suppl 2):S128–34.PubMedCrossRef Hu F, Zhu D, Wang F, Wang M. Current status and trends of antibacterial resistance in China. Clin Infect Dis. 2018;67(Suppl 2):S128–34.PubMedCrossRef
4.
go back to reference China Antimicrobial Resistance Surveillance System. Surveillance of bacterial resistance in children and newborns across China from 2014 to 2017. Zhonghua Yi Xue Za Zhi. 2018;98:3279–87 (in Chinese). China Antimicrobial Resistance Surveillance System. Surveillance of bacterial resistance in children and newborns across China from 2014 to 2017. Zhonghua Yi Xue Za Zhi. 2018;98:3279–87 (in Chinese).
5.
go back to reference David MZ, Boyle-Vavra S, Zychowski DL, Daum RS. Methicillin-susceptible Staphylococcus aureus as a predominantly healthcare-associated pathogen: a possible reversal of roles? PLoS One. 2011;6:e18217.PubMedPubMedCentralCrossRef David MZ, Boyle-Vavra S, Zychowski DL, Daum RS. Methicillin-susceptible Staphylococcus aureus as a predominantly healthcare-associated pathogen: a possible reversal of roles? PLoS One. 2011;6:e18217.PubMedPubMedCentralCrossRef
6.
go back to reference Ikonomidis A, Vasdeki A, Kristo I, Maniatis AN, Tsakris A, Malizos KN, et al. Association of biofilm formation and methicillin-resistance with accessory gene regulator (agr) loci in Greek Staphylococcus aureus clones. Microb Pathog. 2009;47:341–4. Ikonomidis A, Vasdeki A, Kristo I, Maniatis AN, Tsakris A, Malizos KN, et al. Association of biofilm formation and methicillin-resistance with accessory gene regulator (agr) loci in Greek Staphylococcus aureus clones. Microb Pathog. 2009;47:341–4.
7.
go back to reference Bronner S, Monteil H, Prevost G. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev. 2004;28:183–200.PubMedCrossRef Bronner S, Monteil H, Prevost G. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev. 2004;28:183–200.PubMedCrossRef
8.
go back to reference Martinez-Garcia S, Ortiz-Garcia CI, Cruz-Aguilar M, Zenteno JC, Murrieta-Coxca JM, Perez-Tapia SM, et al. Competition/antagonism associations of biofilm formation among Staphylococcus epidermidis Agr groups I, II, and III. J Microbiol. 2019;57:143–53.PubMedCrossRef Martinez-Garcia S, Ortiz-Garcia CI, Cruz-Aguilar M, Zenteno JC, Murrieta-Coxca JM, Perez-Tapia SM, et al. Competition/antagonism associations of biofilm formation among Staphylococcus epidermidis Agr groups I, II, and III. J Microbiol. 2019;57:143–53.PubMedCrossRef
9.
go back to reference Holtfreter S, Grumann D, Schmudde M, Nguyen HT, Eichler P, Strommenger B, et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol. 2007;45:2669–80.PubMedPubMedCentralCrossRef Holtfreter S, Grumann D, Schmudde M, Nguyen HT, Eichler P, Strommenger B, et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol. 2007;45:2669–80.PubMedPubMedCentralCrossRef
10.
go back to reference Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70:631–41.PubMedPubMedCentralCrossRef Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70:631–41.PubMedPubMedCentralCrossRef
11.
go back to reference Carrillo-Marquez MA, Hulten KG, Hammerman W, Lamberth L, Mason EO, Kaplan SL. Staphylococcus aureus pneumonia in children in the era of community-acquired methicillin-resistance at Texas Children’s Hospital. Pediatr Infect Dis J. 2011;30:545–50.PubMedCrossRef Carrillo-Marquez MA, Hulten KG, Hammerman W, Lamberth L, Mason EO, Kaplan SL. Staphylococcus aureus pneumonia in children in the era of community-acquired methicillin-resistance at Texas Children’s Hospital. Pediatr Infect Dis J. 2011;30:545–50.PubMedCrossRef
12.
go back to reference Diagnosis and treatment in children with acute tonsillitis. clinical practice guideline (2016). Chin J Pract Pediatr. 2017;32:161–4 (in Chinese). Diagnosis and treatment in children with acute tonsillitis. clinical practice guideline (2016). Chin J Pract Pediatr. 2017;32:161–4 (in Chinese).
13.
go back to reference Wang X, Shen Y, Huang W, Zhou Y. Characterisation of community-acquired Staphylococcus aureus causing skin and soft tissue infections in a children’s hospital in Shanghai. China Epidemiol Infect. 2019;147:e323.PubMedCrossRef Wang X, Shen Y, Huang W, Zhou Y. Characterisation of community-acquired Staphylococcus aureus causing skin and soft tissue infections in a children’s hospital in Shanghai. China Epidemiol Infect. 2019;147:e323.PubMedCrossRef
14.
go back to reference Hulten KG, Mason EO, Lamberth LB, Forbes AR, Revell PA, Kaplan SL. Analysis of invasive community-acquired methicillin-susceptible Staphylococcus aureus infections during a period of declining community acquired methicillin-resistant Staphylococcus aureus infections at a large children’s hospital. Pediatr Infect Dis J. 2018;37:235–41.PubMedCrossRef Hulten KG, Mason EO, Lamberth LB, Forbes AR, Revell PA, Kaplan SL. Analysis of invasive community-acquired methicillin-susceptible Staphylococcus aureus infections during a period of declining community acquired methicillin-resistant Staphylococcus aureus infections at a large children’s hospital. Pediatr Infect Dis J. 2018;37:235–41.PubMedCrossRef
15.
go back to reference Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann Clin Microbiol Antimicrob. 2010;9:23.PubMedPubMedCentralCrossRef Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann Clin Microbiol Antimicrob. 2010;9:23.PubMedPubMedCentralCrossRef
16.
go back to reference Petersson AC, Olsson-Liljequist B, Miörner H, Haeggman S. Evaluating the usefulness of spa typing, in comparison with pulsed-field gel electrophoresis, for epidemiological typing of methicillin-resistant Staphylococcus aureus in a low-prevalence region in Sweden 2000–2004. Clin Microbiol Infect. 2010;16:456–62.PubMedCrossRef Petersson AC, Olsson-Liljequist B, Miörner H, Haeggman S. Evaluating the usefulness of spa typing, in comparison with pulsed-field gel electrophoresis, for epidemiological typing of methicillin-resistant Staphylococcus aureus in a low-prevalence region in Sweden 2000–2004. Clin Microbiol Infect. 2010;16:456–62.PubMedCrossRef
17.
go back to reference Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, twenty-ninth informational supplement; M100–S29. Wayne: Clin Lab Stand Institute; 2019. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, twenty-ninth informational supplement; M100–S29. Wayne: Clin Lab Stand Institute; 2019.
18.
go back to reference Li SP, Sun J, Zhang JZ, Li XM, Tao XX, Wang LJ, et al. Comparative analysis of the virulence characteristics of epidemic methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from Chinese children: ST59 MRSA highly expresses core gene-encoded toxin. APMIS. 2014;122:101–14.PubMedCrossRef Li SP, Sun J, Zhang JZ, Li XM, Tao XX, Wang LJ, et al. Comparative analysis of the virulence characteristics of epidemic methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from Chinese children: ST59 MRSA highly expresses core gene-encoded toxin. APMIS. 2014;122:101–14.PubMedCrossRef
19.
go back to reference Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38:1008–15.PubMedPubMedCentralCrossRef Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38:1008–15.PubMedPubMedCentralCrossRef
20.
go back to reference Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JA, Kreiswirth BN. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol. 2004;42:792–9.PubMedPubMedCentralCrossRef Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JA, Kreiswirth BN. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol. 2004;42:792–9.PubMedPubMedCentralCrossRef
21.
go back to reference Milheirico C, Oliveira DC, de Lencastre H. Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: “SCCmec IV multiplex”. J Antimicrob Chemother. 2007;60:42–8.PubMedCrossRef Milheirico C, Oliveira DC, de Lencastre H. Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: “SCCmec IV multiplex”. J Antimicrob Chemother. 2007;60:42–8.PubMedCrossRef
22.
go back to reference Gilot P, Lina G, Cochard T, Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 2002;40:4060–7.PubMedPubMedCentralCrossRef Gilot P, Lina G, Cochard T, Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 2002;40:4060–7.PubMedPubMedCentralCrossRef
23.
go back to reference Ote I, Taminiau B, Duprez JN, Dizier I, Mainil JG. Genotypic characterization by polymerase chain reaction of Staphylococcus aureus isolates associated with bovine mastitis. Vet Microbiol. 2011;153:285–92.PubMedCrossRef Ote I, Taminiau B, Duprez JN, Dizier I, Mainil JG. Genotypic characterization by polymerase chain reaction of Staphylococcus aureus isolates associated with bovine mastitis. Vet Microbiol. 2011;153:285–92.PubMedCrossRef
24.
go back to reference Pereyra EAL, Picech F, Renna MS, Baravalle C, Andreotti CS, Russi R, et al. Detection of Staphylococcus aureus adhesion and biofilm-producing genes and their expression during internalization in bovine mammary epithelial cells. Vet Microbiol. 2016;183:69–77.PubMedCrossRef Pereyra EAL, Picech F, Renna MS, Baravalle C, Andreotti CS, Russi R, et al. Detection of Staphylococcus aureus adhesion and biofilm-producing genes and their expression during internalization in bovine mammary epithelial cells. Vet Microbiol. 2016;183:69–77.PubMedCrossRef
25.
go back to reference Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol. 2003;41:4465–7.PubMedPubMedCentralCrossRef Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol. 2003;41:4465–7.PubMedPubMedCentralCrossRef
26.
go back to reference Suryadevara M, Clark AE, Wolk DM, Carman A, Rosenbaum PF, Shaw J. Molecular characterization of invasive Staphylococcus aureus infection in central New York children: importance of two clonal groups and inconsistent presence of selected virulence determinants. J Pediatric Infect Dis Soc. 2013;2:30–9.PubMedCrossRef Suryadevara M, Clark AE, Wolk DM, Carman A, Rosenbaum PF, Shaw J. Molecular characterization of invasive Staphylococcus aureus infection in central New York children: importance of two clonal groups and inconsistent presence of selected virulence determinants. J Pediatric Infect Dis Soc. 2013;2:30–9.PubMedCrossRef
27.
go back to reference Yang Y, Hu Z, Shang W, Hu Q, Zhu J, Yang J, et al. Molecular and phenotypic characterization revealed high prevalence of multidrug-resistant methicillin-susceptible Staphylococcus aureus in Chongqing. Southwestern China Microb Drug Resist. 2017;23:241–6.PubMedCrossRef Yang Y, Hu Z, Shang W, Hu Q, Zhu J, Yang J, et al. Molecular and phenotypic characterization revealed high prevalence of multidrug-resistant methicillin-susceptible Staphylococcus aureus in Chongqing. Southwestern China Microb Drug Resist. 2017;23:241–6.PubMedCrossRef
28.
go back to reference Wu D, Li X, Yang Y, Zheng Y, Wang C, Deng L, et al. Superantigen gene profiles and presence of exfoliative toxin genes in community-acquired meticillin-resistant Staphylococcus aureus isolated from Chinese children. J Med Microbiol. 2011;60:35–45.PubMedCrossRef Wu D, Li X, Yang Y, Zheng Y, Wang C, Deng L, et al. Superantigen gene profiles and presence of exfoliative toxin genes in community-acquired meticillin-resistant Staphylococcus aureus isolated from Chinese children. J Med Microbiol. 2011;60:35–45.PubMedCrossRef
29.
go back to reference Monecke S, Slickers P, Ehricht R. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol. 2008;53:237–51.PubMedCrossRef Monecke S, Slickers P, Ehricht R. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol. 2008;53:237–51.PubMedCrossRef
30.
go back to reference Robinson DA, Monk AB, Cooper JE, Feil EJ, Enright MC. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J Bacteriol. 2005;187:8312–21.PubMedPubMedCentralCrossRef Robinson DA, Monk AB, Cooper JE, Feil EJ, Enright MC. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J Bacteriol. 2005;187:8312–21.PubMedPubMedCentralCrossRef
31.
go back to reference Li J, Wang L, Ip M, Sun M, Sun J, Huang G, et al. Molecular and clinical characteristics of clonal complex 59 methicillin-resistant Staphylococcus aureus infections in Mainland China. PLoS One. 2013;8:e70602.PubMedPubMedCentralCrossRef Li J, Wang L, Ip M, Sun M, Sun J, Huang G, et al. Molecular and clinical characteristics of clonal complex 59 methicillin-resistant Staphylococcus aureus infections in Mainland China. PLoS One. 2013;8:e70602.PubMedPubMedCentralCrossRef
32.
go back to reference Liu X, Liang J, Jiang Y, Wang B, Yuan H, Zhang L, et al. Molecular characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains isolated from outpatients with skin and soft tissue infections in Wuhan. China Pathog Dis. 2016;74:ftw026.PubMedCrossRef Liu X, Liang J, Jiang Y, Wang B, Yuan H, Zhang L, et al. Molecular characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains isolated from outpatients with skin and soft tissue infections in Wuhan. China Pathog Dis. 2016;74:ftw026.PubMedCrossRef
33.
go back to reference Huh K, Chung DR. Changing epidemiology of community-associated methicillin-resistant Staphylococcus aureus in the Asia-Pacific region. Expert Rev Anti Infect Ther. 2016;14:1007–22.PubMedCrossRef Huh K, Chung DR. Changing epidemiology of community-associated methicillin-resistant Staphylococcus aureus in the Asia-Pacific region. Expert Rev Anti Infect Ther. 2016;14:1007–22.PubMedCrossRef
34.
go back to reference Gu FF, Chen Y, Dong DP, Song Z, Guo XK, Ni YX, et al. Molecular epidemiology of Staphylococcus aureus among patients with skin and soft tissue infections in two Chinese hospitals. Chin Med J (Engl). 2016;129:2319–24.CrossRef Gu FF, Chen Y, Dong DP, Song Z, Guo XK, Ni YX, et al. Molecular epidemiology of Staphylococcus aureus among patients with skin and soft tissue infections in two Chinese hospitals. Chin Med J (Engl). 2016;129:2319–24.CrossRef
35.
go back to reference van Leeuwen W, van Nieuwenhuizen W, Gijzen C, Verbrugh H, van Belkum A. Population studies of methicillin-resistant and -sensitive Staphylococcus aureus strains reveal a lack of variability in the agrD gene, encoding a staphylococcal autoinducer peptide. J Bacteriol. 2000;182:5721–9.PubMedPubMedCentralCrossRef van Leeuwen W, van Nieuwenhuizen W, Gijzen C, Verbrugh H, van Belkum A. Population studies of methicillin-resistant and -sensitive Staphylococcus aureus strains reveal a lack of variability in the agrD gene, encoding a staphylococcal autoinducer peptide. J Bacteriol. 2000;182:5721–9.PubMedPubMedCentralCrossRef
36.
go back to reference Azmi K, Qrei W, Abdeen Z. Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of Staphylococcus aureus isolated from Palestinian patients. Bmc Genomics. 2019;20:578.PubMedPubMedCentralCrossRef Azmi K, Qrei W, Abdeen Z. Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of Staphylococcus aureus isolated from Palestinian patients. Bmc Genomics. 2019;20:578.PubMedPubMedCentralCrossRef
37.
go back to reference Tahmasebi H, Dehbashi S, Arabestani MR. Association between the accessory gene regulator (agr) locus and the presence of superantigen genes in clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes. 2019;12:130.PubMedPubMedCentralCrossRef Tahmasebi H, Dehbashi S, Arabestani MR. Association between the accessory gene regulator (agr) locus and the presence of superantigen genes in clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes. 2019;12:130.PubMedPubMedCentralCrossRef
38.
go back to reference Chong YP, Kim ES, Park SJ, Park KH, Kim T, Kim MN, et al. Accessory gene regulator (agr) dysfunction in Staphylococcus aureus bloodstream isolates from South Korean patients. Antimicrob Agents Chemother. 2013;57:1509–12.PubMedPubMedCentralCrossRef Chong YP, Kim ES, Park SJ, Park KH, Kim T, Kim MN, et al. Accessory gene regulator (agr) dysfunction in Staphylococcus aureus bloodstream isolates from South Korean patients. Antimicrob Agents Chemother. 2013;57:1509–12.PubMedPubMedCentralCrossRef
39.
go back to reference Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A. 2002;99:7687–92.PubMedPubMedCentralCrossRef Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A. 2002;99:7687–92.PubMedPubMedCentralCrossRef
40.
go back to reference Wright JS 3rd, Traber KE, Corrigan R, Benson SA, Musser JM, Novick RP. The agr radiation: an early event in the evolution of staphylococci. J Bacteriol. 2005;187:5585–94.PubMedPubMedCentralCrossRef Wright JS 3rd, Traber KE, Corrigan R, Benson SA, Musser JM, Novick RP. The agr radiation: an early event in the evolution of staphylococci. J Bacteriol. 2005;187:5585–94.PubMedPubMedCentralCrossRef
41.
go back to reference Robinson DA, Enright MC. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2003;47:3926–34.PubMedPubMedCentralCrossRef Robinson DA, Enright MC. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2003;47:3926–34.PubMedPubMedCentralCrossRef
42.
go back to reference Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis. 2003;9:978–84.PubMedPubMedCentralCrossRef Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis. 2003;9:978–84.PubMedPubMedCentralCrossRef
43.
go back to reference Cucarella C, Tormo MA, Knecht E, Amorena B, Lasa I, Foster TJ, et al. Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infect Immun. 2002;70:3180–6.PubMedPubMedCentralCrossRef Cucarella C, Tormo MA, Knecht E, Amorena B, Lasa I, Foster TJ, et al. Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infect Immun. 2002;70:3180–6.PubMedPubMedCentralCrossRef
44.
go back to reference Mottola C, Semedo-Lemsaddek T, Mendes JJ, Melo-Cristino J, Tavares L, Cavaco-Silva P, et al. Molecular typing, virulence traits and antimicrobial resistance of diabetic foot staphylococci. J Biomed Sci. 2016;23:33.PubMedPubMedCentralCrossRef Mottola C, Semedo-Lemsaddek T, Mendes JJ, Melo-Cristino J, Tavares L, Cavaco-Silva P, et al. Molecular typing, virulence traits and antimicrobial resistance of diabetic foot staphylococci. J Biomed Sci. 2016;23:33.PubMedPubMedCentralCrossRef
45.
go back to reference Monecke S, Ludicke C, Slickers P, Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis. 2009;28:1159–65.PubMedCrossRef Monecke S, Ludicke C, Slickers P, Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis. 2009;28:1159–65.PubMedCrossRef
46.
go back to reference Vautor E, Magnone V, Rios G, Le Brigand K, Bergonier D, Lina G, et al. Genetic differences among Staphylococcus aureus isolates from dairy ruminant species: a single-dye DNA microarray approach. Vet Microbiol. 2009;133:105–14.PubMedCrossRef Vautor E, Magnone V, Rios G, Le Brigand K, Bergonier D, Lina G, et al. Genetic differences among Staphylococcus aureus isolates from dairy ruminant species: a single-dye DNA microarray approach. Vet Microbiol. 2009;133:105–14.PubMedCrossRef
Metadata
Title
Clinical and molecular characteristics of Staphylococcus aureus isolated from Chinese children: association among the agr groups and genotypes, virulence genes and disease types
Authors
Yan Xu
Su-Yun Qian
Kai-Hu Yao
Fang Dong
Wen-Qi Song
Chen Sun
Xin Yang
Jing- Hui Zhen
Xi-Qing Liu
Zhi -Yong Lv
Xi Yang
Publication date
01-04-2021
Publisher
Springer Singapore
Published in
World Journal of Pediatrics / Issue 2/2021
Print ISSN: 1708-8569
Electronic ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-021-00421-4

Other articles of this Issue 2/2021

World Journal of Pediatrics 2/2021 Go to the issue