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Detection of cross-infection associated to a Brazilian PCR-ribotype of Clostridium difficile in a university hospital in Rio de Janeiro, Brazil

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Abstract

Clostridium difficile is an important nosocomial enteric pathogen and is the etiological agent of pseudomembranous colites. Recently, the rates of C. difficile infection (CDI) have increased worldwide, but in Brazil few data about this situation and the incidence of clonal types of C. difficile exist. This study aimed to isolate and characterize C. difficile strains from samples obtained of a university hospital (HUCFF) in Rio de Janeiro city, Brazil. CDI was identified by ELISA in 27.1% of HUCFF-in-patients enrolled in the study, and the bacterium was recovered from eight of these fecal samples. All strains, except one, presented tcdA and tcdB genes and presented neither the cdtA and cdtB genes nor any significant deletions in the tcdC gene. All strains were sensitive to metronidazole, vancomycin and moxifloxacin, and resistant to clindamycin, ciprofloxacin and levofloxacin. PCR-ribotyping and PFGE revealed four different clonal types among the isolates. The Brazilian PCR-ribotype 133 accounted for 50% of strains isolated, and PCR-ribotype 233 strains were obtained from 25% of the in-patients. The prevalence and resurgence of the Brazilian PCR-ribotype 133 among the hospitalized patients of HUCFF was established, and cross-infection of different patients associated to the same PCR-ribotypes was detected. Our results emphasize the importance of the diagnosis and control of CDI in order to prevent the emergence of specific clones that can lead to C. difficile-associated outbreaks in Brazilian hospitals.

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References

  • Ackermann G, Tang-Feldman YJ, Schaumann R, Henderson JP, Rodloff AC, Silva J Jr, Cohen SH (2003) Antecedent use of fluoroquinolones is associated with resistance to moxifloxacin in Clostridium difficile. Clin Microbiol Infect 9:526–530

    Article  CAS  PubMed  Google Scholar 

  • Akerlund T, Persson I, Unemo M, Norén T, Svenungsson B, Wullt M, Burman LG (2008) Increased sporulation rate of epidemic Clostridium difficile Type 027/NAP1. J Clin Microbiol 46(4):1530–1533

    Article  PubMed  Google Scholar 

  • Alcides AP, Brazier JS, Pinto LJ, Balassiano IT, Boente RF, de Paula GR, Ferreira EO, Avelar KES, Miranda KR, Ferreira MCS, Domingues RMCP (2007) New PCR ribotypes of Clostridium difficile detected in children in Brazil: prevalent types of Clostridium difficile in Brazil. Antonie Van Leeuwenhoek 92(1):53–59

    Article  PubMed  Google Scholar 

  • Balassiano IT, Miranda KR, Boente RF, Pauer H, Oliveira ICM, Santos-Filho J, Amorim ELT, Caniné GA, Souza CF, Gomes MZR, Ferreira EO, Brazier JS, Domingues RMCP (2009) Characterization of Clostridium difficile strains isolated from immunosuppressed inpatients in a hospital in Rio de Janeiro, Brazil. Anaerobe 15:61–64

    Article  CAS  PubMed  Google Scholar 

  • Barbut F, Decré D, Lalande V, Burghoffer B, Noussair L, Gigandon A, Espinasse F, Raskine L, Robert J, Mangeol A, Branger C, Petit JC (2005) Clinical features of Clostridium difficile-associated diarrhoea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J Med Microbiol 54(Pt 2):181–185

    Article  CAS  PubMed  Google Scholar 

  • Barbut F, Mastrantonio P, Delmeé M, Brazier J, Kuijper J, Poxton I (2007) Prospective study of Clostridium difficile infections in Europe phenotypic and genotypic characterisation of the isolates. Clin Microbiol Infect 13(11):1048–1057

    Article  CAS  PubMed  Google Scholar 

  • Bourgault AM, Lamothe F, Loo VG, Poirier L, CDAD-CSI Study Group (2006) In vitro susceptibility of Clostridium difficile clinical isolates from a multi-institutional outbreak in Southern Québec, Canada. Antimicrob Agents Chemother 50(10):3473–3475

    Article  CAS  PubMed  Google Scholar 

  • Carman RJ, Genheimer CW, Rafii F, Park M, Hiltonsmith MF, Lyerly DM (2009) Diversity of moxifloxacin resistance during a nosocomial outbreak of a predominantly ribotype ARU 027 Clostridium difficile diarrhea. Anaerobe 15:244–248

    Article  CAS  PubMed  Google Scholar 

  • Clinical and Laboratory Standards Institute (2007) Performance standards for antimicrobial susceptibility testing. Sixteenth informational supplement. Document M100-S16. Wayne, PA

  • Curry SR, Marsh JW, Shutt KA, Muto CA, O’Leary MM, Saul MI, Pasculle AW, Harrison LH (2009) High frequency of rifampin resistance identified in an epidemic Clostridium difficile clone from a large teaching hospital. Clin Infect Dis 48(4):425–429

    Article  CAS  PubMed  Google Scholar 

  • Dridi L, Tankovic J, Burghoffer B, Barbut F, Petit JC (2002) gyrA and gyrB mutations are implicated in cross-resistance to ciprofloxacin and moxifloxacin in Clostridium difficile. Antimicrob Agents Chemother 46(11):3418–3421

    Article  CAS  PubMed  Google Scholar 

  • Hammond GA, Lyerly DM, Johnson JL (1997) Transcriptional analysis of the toxigenic element of Clostridium difficile. Microb Pathog 22:143–154

    Article  CAS  PubMed  Google Scholar 

  • Hookman P, Barkin JS (2009) Clostridium difficile associated infection, diarrhea and colitis. World J Gastroenterol 15(13):1554–1580

    Article  PubMed  Google Scholar 

  • Huang H, Wu S, Wang M, Zhang Y, Fang H, Palmgren AC, Weintraub A, Nord CE (2009a) Clostridium difficile infections in a Shanghai hospital: antimicrobial resistance, toxin profiles and ribotypes. Int J Antimicrob Agents 33(4):339–342

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Weintraub A, Fang H, Nord CE (2009b) Antimicrobial resistance in Clostridium difficile. Int J Antimicrob Agents 34:516–522

    Article  CAS  PubMed  Google Scholar 

  • Jousimies-Somer HR, Summanen P, Citron DM, Baron EJ, Wexler HM, Finegold SM (2002) Anaerobic bacteriology manual, 6th edn. Star Publishing Company, Belmont, CA

    Google Scholar 

  • Kononen E, Rasinpera M, Virolainen A, Mentula S, Lyytikainen O (2009) Diagnostic trends in Clostridium difficile detection in Finnish microbiology laboratories. Anaerobe 15:261–265

    Article  PubMed  Google Scholar 

  • Kuijper EJ, Coignard B, Brazier JS, Suetens C, Drudy D, Wiuff C, Pituch H, Reichert P, Schneider F, Widmer AF, Olsen KE, Allerberger F, Notermans DW, Barbut F, Delmée M, Wilcox M, Pearson A, Patel BC, Brown DJ, Frei R, Akerlund T, Poxton IR, Tüll P (2007) Update of Clostridium difficile-associated disease due to PCR ribotype 027 in Europe. Euro Surveill 12(6):E1–E2

    CAS  PubMed  Google Scholar 

  • Lemee L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, Pons LJ (2004) Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (toxin A), and tcdB genes for toxigenic culture of Clostrdium difficile. J Clin Microbiol 42:5710–5714

    Article  CAS  PubMed  Google Scholar 

  • Martin H, Willey B, Low DE, Staempfli HR, McGeer A, Boerlin P, Mulvey M, Weese JS (2006) Characterization of Clostridium difficile strains isolated from patients in Ontario, Canada, from 2004 to 2006. J Clin Microbiol 46(9):2999–3004

    Article  Google Scholar 

  • Mathis JM, Pilkinton L, McMillin DE (1999) Detection and transcription of toxin DNA in a nontoxigenic strain of Clostridium difficile. Curr Microbiol 38:324–328

    Article  CAS  PubMed  Google Scholar 

  • Maurelli AT (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267:1–8

    Article  CAS  PubMed  Google Scholar 

  • Mutlu E, Wroe AJ, Sanchez-Hurtado C, Brazier JS, Poxton I (2007) Molecular characterization and antimicrobial susceptibility patterns of Clostridium difficile strains isolated from hospitals in south-east Scotland. J Med Microbiol 56:921–929

    Article  CAS  PubMed  Google Scholar 

  • Pinto LJF, Alcides APP, Ferreira EO, Avelar KES, Sabrá A, Domingues RMCP, Ferreira MCS (2003) Incidence and importance of Clostridium difficile in paediatric diarrhoea in Brazil. J Med Microbiol 52:1095–1099

    Article  CAS  PubMed  Google Scholar 

  • Pituch H, Brazier JS, Obuch-Woszczatynski P, Wultanska D, Meisel-Mikolajczyk F, Luczak M (2006) Prevalence and association of PCR ribotypes of Clostridium difficile isolated from symptomatic patients from Warsaw with macrolide-lincosamide-streptogramin B (MLSB) type resistance. J Med Microbiol 55:207–213

    Article  CAS  PubMed  Google Scholar 

  • Quesada-Gómez C, Rodríguez C, Gamboa-Coronado MD, Rodríguez-Cavallini E, Du T, Mulvey MR, Villalobos-Zúñiga M, Boza-Cordero R (2010) Emergence of Clostridium difficile NAP1 in Latin America. J Clin Microbiol 48(2):669–670

    Article  PubMed  Google Scholar 

  • Rupnik M, Wilcox MH, Gerding DN (2009) Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7(7):526–536

    Article  CAS  PubMed  Google Scholar 

  • Sawabe E, Kato H, Osawa K, Chida T, Tojo N, Arakawa Y, Okamura N (2007) Molecular analysis of Clostridium difficile at a university teaching hospital in Japan: a shift in the predominant type over a five-year period. Eur J Clin Microbiol Infect Dis 26(10):695–703

    Article  CAS  PubMed  Google Scholar 

  • Schroeder MS (2005) Clostridium difficile-associated diarrhea. Am Fam Physician 71(5):921–928

    PubMed  Google Scholar 

  • Sokurenko EV, Hasty DL, Dykhuizen DE (1999) Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol 7(5):191–195

    Article  CAS  PubMed  Google Scholar 

  • Spigaglia P, Mastrantonio P (2004) Comparative analysis of Clostridium difficile clinical isolates belonging to different genetic lineages and time periods. J Med Microbiol 53:1129–1136

    Article  CAS  PubMed  Google Scholar 

  • Spigaglia P, Barbanti F, Mastrantonio P, Brazier JS, Barbut F, Delmée M, Kuijper E, Poxton IR, European Study Group on Clostridium difficile (ESGCD) (2008) Fluoroquinolone resistance in Clostridium difficile isolates from a prospective study of C. difficile infections in Europe. J Med Microbiol 57(Pt 6):784–789

    Article  CAS  PubMed  Google Scholar 

  • Stabler RA, He M, Dawson L, Martin M, Valiente E, Corton C, Lawley TD, Sebaihia M, Quail MA, Rose G, Gerding DN, Gibert M, Popoff MR, Parkhill J, Dougan G, Wren BW (2009) Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol 10(9):R102

    Article  PubMed  Google Scholar 

  • Stubbs SLJ, Brazier JS, O’Neill GL, Duerden BI (1999) PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 37:461–463

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Angela Thompson, Centers for Disease Control/Atlanta, for kindly providing the NAP1/027 C. difficile strain. The authors are also thankful to Rosane Ferro Trindade, for technical support, and to Dr. Edwin A. Yates for reviewing the text. This work was supported by the following national institutions: CNPq, FAPERJ, PRONEX.

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Authors and Affiliations

  1. Laboratório de Biologia de Anaeróbios—Instituto de Microbiologia Prof. Paulo de Góes—Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro—Cidade Universitária, Rio de Janeiro, CEP 21941-590, Brazil

    Ilana T. Balassiano, Joaquim dos Santos-Filho & Regina M. C. P. Domingues

  2. Laboratório de Zoonoses Bacterianas, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil

    Ilana T. Balassiano & Juliana M. Vital-Brazil

  3. Coordenação de Controle de Infecções Hospitalares, Hospital Universitário Clementino Fraga Filho, UFRJ, Rio de Janeiro, RJ, Brazil

    Simone A. Nouér & Claudia R. C. Souza

  4. Escola de Medicina, UFRJ, Rio de Janeiro, RJ, Brazil

    Simone A. Nouér

  5. Anaerobe Reference Unit, University Hospital of Wales, Cardiff, UK

    Jon S. Brazier

  6. Instituto de Microbiologia Professor Paulo de Góes, UFRJ, Xerém, RJ, Brazil

    Eliane de O. Ferreira

Authors
  1. Ilana T. Balassiano
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  2. Joaquim dos Santos-Filho
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  3. Juliana M. Vital-Brazil
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  4. Simone A. Nouér
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  5. Claudia R. C. Souza
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  6. Jon S. Brazier
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  7. Eliane de O. Ferreira
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  8. Regina M. C. P. Domingues
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Correspondence to Ilana T. Balassiano.

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Balassiano, I.T., Santos-Filho, J.d., Vital-Brazil, J.M. et al. Detection of cross-infection associated to a Brazilian PCR-ribotype of Clostridium difficile in a university hospital in Rio de Janeiro, Brazil. Antonie van Leeuwenhoek 99, 249–255 (2011). https://doi.org/10.1007/s10482-010-9483-8

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  • DOI: https://doi.org/10.1007/s10482-010-9483-8

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