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Bacteriology

Quinolone-Resistant Escherichia coli O127a:K63 Serotype with an Extended-Spectrum-Beta-Lactamase Phenotype from a Food Poisoning Outbreak in China

Rongzhang Hao, Shaofu Qiu, Yong Wang, Guang Yang, Wenli Su, Lixue Song, Jia Zhang, Jiaxu Chen, Leili Jia, Ligui Wang, Hongbin Song
Rongzhang Hao
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Shaofu Qiu
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Yong Wang
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Guang Yang
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Wenli Su
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Lixue Song
bThe Military General Hospital of Beijing PLA, Beijing, China
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Jia Zhang
cInstitute of Parasitic Diseases, Chinese Center of Disease Control and Prevention, Shanghai, China
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Jiaxu Chen
cInstitute of Parasitic Diseases, Chinese Center of Disease Control and Prevention, Shanghai, China
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Leili Jia
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Ligui Wang
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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Hongbin Song
aInstitute of Disease Control and Prevention, Academy of Military Medical Sciences, Beijing, China
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DOI: 10.1128/JCM.00276-12
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ABSTRACT

We report an atypical enteropathogenic Escherichia coli O127a:K63 strain with resistance to quinolones and extended-spectrum cephalosporins isolated from a 2010 food poisoning outbreak involving 112 adults in China. Two resistance genes [bla CTX-M-15, aac(6′)-Ib-c] and five mutations (two in gyrA, two in parC, one in parE) coexisted in this enteropathogenic E. coli strain.

TEXT

Food poisoning from multidrug-resistant strains of diarrheagenic Escherichia coli has received considerable public attention, especially since the large outbreak of hemolytic uremic syndrome caused by E. coli O104:H4 in Germany in 2011 (12). Extended-spectrum cephalosporins and quinolones are widely used for diarrheagenic E. coli, but E. coli isolates are increasingly resistant to these antimicrobials (11). Here, we report the isolation of an E. coli strain harboring virulence genes and genes conferring resistance to quinolones and extended-spectrum cephalosporins from a 2010 food poisoning outbreak involving 112 adult students in China.

On 16 September 2010, 112 students (18 to 23 years old) from a university in Zhengzhou, China, experienced diarrhea and other enterogastritis symptoms after eating in the same dining room the previous evening. Seventy-eight (70%) students were hospitalized, and 27 of these students experienced serious symptoms, including stomachache, fever, vomiting, and watery diarrhea (>5 times/day). Twenty-eight stool specimens were collected from these 27 inpatients within 24 h after admission for laboratory testing. The suspected pathogenic bacteria were isolated through standard procedures on conventional selective media, and the isolated strains were identified using a commercial biochemical test (API 20E system; bioMérieux Vitek, France). Serotyping was carried out by slide agglutination with a conventional E. coli antiserum kit (Denka Seiken, Tokyo, Japan). Sixteen strains of enteropathogenic E. coli serotype O127a:K63 were isolated from the stool specimens. Results of epidemiologic investigation and laboratory tests indicated that this food poisoning outbreak was due to the enteropathogenic E. coli O127a:K63.

One 20-year-old male patient had especially severe symptoms, including persistent abdominal cramps with severe paroxysmal pain and abnormal blood test results. Between 16 September and 27 September, he was hospitalized twice for diarrhea. His symptoms were controlled with intravenous administration of levofloxacin and cefpiramide sodium and supportive treatment, and he was released from the hospital. We followed up with this patient for 1 year and found that he often experienced stomachaches, hiccups, nausea, and other symptoms of chronic enterogastritis. Further clinical investigation excluded other chronic or immune-related diseases (e.g., cancer, hepatitis, and HIV infection); therefore, the chronic enterogastritis appeared to be related to the food poisoning caused by enteropathogenic E. coli.

The two suspected isolates obtained from stool specimens during this patient's hospitalizations were identified as enteropathogenic E. coli serotype O127a:K63, which was the same isolate obtained from 14 other inpatients who had serious symptoms. All 16 isolates were screened for virulence factors, including eae, stx, bfpA, and the E. coli adherence factor (EAF) plasmid, using PCR assays that have been described previously (1, 2). Reference strains of enteropathogenic E. coli (EPEC) and enterohemorrhagic E. coli harboring these virulence genes were used as positive controls. Antimicrobial susceptibility was tested by the disk diffusion method according to the Clinical and Laboratory Standards Institute guidelines, and MICs of ciprofloxacin, norfloxacin, cefotaxime, ceftriaxone, and nalidixic acid were determined by Etest strips (AB Biodisk, Solna, Sweden); E. coli ATCC 25922 was used as the quality control organism. Resistance genes gyrA, gyrB, parC, parE, qnr, acc, blaTEM, and blaCTX-M were detected using previously described PCR methods (4, 5, 8). Bidirectional sequence data were obtained for these resistance and virulence genes.

The PCR and sequencing results indicated that the E. coli isolate harbored the virulence gene eae, which encodes the outer membrane protein intimin but not stx, bfpA, or the EAF plasmid, suggesting an atypical EPEC (6). Antimicrobial susceptibility tests showed that the isolates were completely resistant to cefotaxime, ceftriaxone, nalidixic acid, norfloxacin, ciprofloxacin, levofloxacin, amoxicillin, ampicillin, gentamicin, trimethoprim-sulfamethoxazole, and tetracycline and intermediately resistant to chloramphenicol but susceptible to imipenem. The results of MIC tests showed high-level resistance to ceftriaxone, cefotaxime, norfloxacin, nalidixic acid, and ciprofloxacin (Table 1). Results of sequence analysis revealed that resistance to quinolone and extended-spectrum cephalosporin was mediated by the following five mutations and two resistance genes: two mutations in gyrA (Ser83→Leu, Asp87→Asn), two mutations in parC (Ser80→Ile, Ala108→Val), one mutation in parE (Ser458→Ala), and resistance genes aac(6′)-Ib-cr and blaCTX-M-15.

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Table 1

Antimicrobial susceptibility profile (MIC) and resistance genes of 16 E. coli O127a:K63 isolates and the ATCC 25922 controla

EPEC causes diarrhea in infants and children (7) but rarely causes disease in adults (9). EPEC infection in adults in this food poisoning outbreak was probably due to the coexistence of eae-encoded intimin and multidrug resistance. Enteropathogenic E. coli O127a strains were primarily isolated from the environment (10), and our study is the first to report clinical isolates of atypical EPEC O127a:K63 serotype obtained from a food poisoning outbreak. In recent decades, an increasing number of E. coli isolates have acquired resistance to quinolones or extended-spectrum cephalosporins (5, 13). However, few studies have described E. coli isolates that simultaneously display resistance to these two antimicrobials, which was primarily due to several ESBL-producing resistant genes (3, 8). In contrast, the E. coli isolates in this study carried more resistant genes [i.e., two mutations in gyrA (Ser83→Leu, Asp87→Asn), two in parC (Ser80→Ile, Ala108→Val), one in parE (Ser458→Ala), and aac(6′)-Ib-cr and blaCTX-M-15], which led to high-level resistance to both quinolones and extended-spectrum cephalosporins.

In conclusion, we report an atypical enteropathogenic E. coli O127a:K63 strain isolated from adults that displayed multidrug resistance, including high-level resistance to both quinolones and extended-spectrum cephalosporins. The emergence of atypical ESBL-producing EPEC with quinolone resistance from adults is problematic because of the difficulties in treatment and infection control. It is therefore important to strengthen surveillance of EPEC strains with multidrug resistance, especially quinolone-resistant ESBL-producing bacteria.

ACKNOWLEDGMENTS

This work was funded by the Mega-projects of Science and Technology Research (grant no. 2012ZX10004215, 2012ZX10004-801, 2011ZX10004-001, and 2009ZX10004-205), the National Natural Science Foundation of China (grant no. 21105122 and 81001267), and the Beijing Science and Technology Nova Program (grant no. 2010B067).

FOOTNOTES

    • Received 29 January 2012.
    • Returned for modification 19 March 2012.
    • Accepted 25 April 2012.
    • Accepted manuscript posted online 2 May 2012.
  • Copyright © 2012, American Society for Microbiology. All Rights Reserved.

REFERENCES

  1. 1.↵
    1. Andrews N,
    2. et al
    . 2000. The European Sero-Epidemiology Network: standardizing the enzyme immunoassay results for measles, mumps and rubella. Epidemiol. Infect. 125:127–141.
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    1. Aranda KR,
    2. Fagundes-Neto U,
    3. Scaletsky IC
    . 2004. Evaluation of multiplex PCRs for diagnosis of infection with diarrheagenic Escherichia coli and Shigella spp. J. Clin. Microbiol. 42:5849–5853.
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    1. Cassier P,
    2. et al
    . 2011. Cephalosporin and fluoroquinolone combinations are highly associated with CTX-M beta-lactamase-producing Escherichia coli: a case-control study in a French teaching hospital. Clin. Microbiol. Infect. 17:1746–1751.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Cattoir V,
    2. Poirel L,
    3. Rotimi V,
    4. Soussy CJ,
    5. Nordmann P
    . 2007. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 60:394–397.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    1. Donaldson SC,
    2. et al
    . 2006. Molecular epidemiology of ceftiofur-resistant Escherichia coli isolates from dairy calves. Appl. Environ. Microbiol. 72:3940–3948.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    1. Hernandes RT,
    2. Elias WP,
    3. Vieira MA,
    4. Gomes TA
    . 2009. An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol. Lett. 297:137–149.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    1. Jensen C,
    2. et al
    . 2007. Attaching and effacing Escherichia coli isolates from Danish children: clinical significance and microbiological characteristics. Clin. Microbiol. Infect. 13:863–872.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Maeda Y,
    2. et al
    . 2011. Molecular characterization and phylogenetic analysis of quinolone resistance-determining regions (QRDRs) of gyrA, gyrB, parC and parE gene loci in viridans group streptococci isolated from adult patients with cystic fibrosis. J. Antimicrob. Chemother. 66:476–486.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    1. Nimri LF,
    2. Meqdam M
    . 2004. Enteropathogens associated with cases of gastroenteritis in a rural population in Jordan. Clin. Microbiol. Infect. 10:634–639.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Pandey M,
    2. et al
    . 2003. Association of cytolethal distending toxin locus cdtB with enteropathogenic Escherichia coli isolated from patients with acute diarrhea in Calcutta, India. J. Clin. Microbiol. 41:5277–5281.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    1. Paterson DL
    . 2006. Resistance in Gram-negative bacteria: Enterobacteriaceae. Am. J. Infect. Control 34:S20–S28; discussion S64-S73.
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.↵
    1. Rohde H,
    2. et al
    . 2011. Open-source genomic analysis of Shiga-toxin-producing E. coli O104:H4. N. Engl. J. Med. 365:718–724.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    1. Siddiqui AA
    . 2008. Prevalence of quinolone-resistant urinary tract infections in Comanche County Memorial Hospital. J. Okla. State Med. Assoc. 101:210–212.
    OpenUrlPubMed
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Quinolone-Resistant Escherichia coli O127a:K63 Serotype with an Extended-Spectrum-Beta-Lactamase Phenotype from a Food Poisoning Outbreak in China
Rongzhang Hao, Shaofu Qiu, Yong Wang, Guang Yang, Wenli Su, Lixue Song, Jia Zhang, Jiaxu Chen, Leili Jia, Ligui Wang, Hongbin Song
Journal of Clinical Microbiology Jun 2012, 50 (7) 2450-2451; DOI: 10.1128/JCM.00276-12

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Quinolone-Resistant Escherichia coli O127a:K63 Serotype with an Extended-Spectrum-Beta-Lactamase Phenotype from a Food Poisoning Outbreak in China
Rongzhang Hao, Shaofu Qiu, Yong Wang, Guang Yang, Wenli Su, Lixue Song, Jia Zhang, Jiaxu Chen, Leili Jia, Ligui Wang, Hongbin Song
Journal of Clinical Microbiology Jun 2012, 50 (7) 2450-2451; DOI: 10.1128/JCM.00276-12
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