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Corynebacterium ulcerans isolates from humans and dogs: fibrinogen, fibronectin and collagen-binding, antimicrobial and PFGE profiles

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Abstract

Corynebacterium ulcerans has been increasingly isolated as an emerging zoonotic agent of diphtheria and other infections from companion animals. Since pets are able to act as symptomless carriers, it is also essential to identify virulence potential for humans of these isolates. In this work the ability of C. ulcerans to bind to fibrinogen (Fbg), fibronectin (Fn) and Type I collagen as well the genetic relationship among strains isolated from human and asymptomatic dogs in Rio de Janeiro (Brazil) were analyzed. Five pulsed-field gel electrophoresis (PFGE) profiles were demonstrated (I, II, III, IV and V). In addition, the IV and V profiles exhibiting ≥85 % similarity were expressed by the BR-AD41 and BR-AD61 strains from companion dogs living in the same neighborhood. Independent of the PFGE-types, human and dog isolates showed affinity to Fbg, Fn and collagen. Heterogeneity of PFGE profiles indicated endemicity of C. ulcerans in the Rio de Janeiro metropolitan area. Differences in the expression of adhesins to the human extracellular matrix may contribute to variations in the virulence and zoonotic potential of C. ulcerans strains.

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References

  • Baio PV, Mota HF, Freitas AD et al (2013) Clonal multidrug-resistant Corynebacterium striatum within a nosocomial environment, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 108:23–29

    Article  CAS  PubMed  Google Scholar 

  • Berger A, Huber I, Merbecks SS et al (2011) Toxigenic Corynebacterium ulcerans in woman and cat. Emerg Infect Dis 17:1767–1768

    Article  PubMed  Google Scholar 

  • Bonnet JM, Begg NT (1999) Control of diphtheria: guidance for consultants in communicable disease control. Commun Dis Public Health 2:242–249

    CAS  PubMed  Google Scholar 

  • Canadian Council on Animal Care (CCAC) (2013) Guidelines on: procurement of animals used in science. http://www.ccac.ca/Documents/Standards/Guidelines/Procurement.pdf. Accessed 10 Mar 2013

  • Centers for Disease Control and Prevention (CDC) (2011) Respiratory diphtheria-like illness caused by toxigenic Corynebacterium ulcerans—Idaho, 2010. MMWR 60:77

  • Centers for Disease Control and Prevention (2012) Health information for international travel. Oxford University Press, New York

  • Clinical Laboratory Standards Institute (CLSI) (2007) Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria, approved guideline. CLSI document M45-A (ISBN 1-56238-607-7:4–6)

  • De Zoysa A, Hawkey PM, Engler K, George R et al (2005) Characterization of toxigenic Corynebacterium ulcerans strains isolated from humans and domestic cats in the United Kingdom. J Clin Microbiol 43:4377–4381

    Article  PubMed Central  PubMed  Google Scholar 

  • Desseau RB, Brandt-Christensen M, Jensen OJ, Tonnesen P (1995) Pulmonary nodules due to Corynebacterium ulcerans. Eur Respir J 8(4):651–653

    Google Scholar 

  • Dewinter LM, Bernard KA, Romney MG (2005) Human clinical isolates of Corynebacterium diphtheriae and Corynebacterium ulcerans collected in Canada from 1999 to 2003 but not fitting reporting criteria for cases of diphtheria. J Clin Microbiol 43:3447–3449

    Article  PubMed Central  PubMed  Google Scholar 

  • Dias AASO, Silva FC Jr, Pereira GA, Souza MC et al (2010) Corynebacterium ulcerans isolated from an asymptomatic dog kept in an animal shelter in the metropolitan area of Rio de Janeiro, Brazil. Vector Borne Zoonotic Dis 10:743–748

    Article  PubMed  Google Scholar 

  • Dias AASO, Santos LS, Sabbadini PS, Santos CS et al (2011a) Corynebacterium ulcerans diphtheria: an emerging zoonosis in Brazil and worldwide. Rev Saúde Pública 45:1176–1191

    Article  PubMed  Google Scholar 

  • Dias AASO, Silva FC Jr, Santos LS, Ribeiro-Carvalho MM et al (2011b) Strain-dependent arthritogenic potential of the zoonotic pathogen Corynebacterium ulcerans. Vet Microbiol 53:323–331

    Article  Google Scholar 

  • Doolittle RF (1984) Fibrinogen and fibrin. Annu Rev Biochem 53:195–229

    Article  CAS  PubMed  Google Scholar 

  • Efstratiou A, George RC (1999) Laboratory guidelines for the diagnosis of infections caused by Corynebacterium diphtheriae and Corynebacterium ulcerans. Commun Dis Public Health 2:250–257

    CAS  PubMed  Google Scholar 

  • Engvall E, Ruoslahti E (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer 20:1–5

    Article  CAS  PubMed  Google Scholar 

  • Engvall E, Ruoslahti E, Miller EJ (1978) Affinity of fibronectin to collagens of different genetic types and to fibrinogen. J Exp Med 147:1584–1595

    Article  CAS  PubMed  Google Scholar 

  • Funke G, Bernard AK (2007) Coryneform Gram-positive rods. In: Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA (eds) Manual of clinical microbiology, 9th edn. ASM Press, Washington, DC, pp 485–514

    Google Scholar 

  • Gaede KI, Heesemann J (1995) Arthritogenicity of genetically manipulated Yersinia enterocolitica serotype O8 for Lewis rats. Infect Immun 63:714–719

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gomes DL, Martins CA, Faria LM, Santos LS et al (2009) Corynebacterium diphtheriae as an emerging pathogen in nephrostomy catheter-related infection: evaluation of traits associated with bacterial virulence. J Med Microbiol 58:1419–1427

    Article  CAS  PubMed  Google Scholar 

  • Harlow E, Lane D (1988) Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Hatanaka A, Tsunoda A, Okamoto M, Ooe K et al (2003) Corynebacterium ulcerans diphtheria in Japan. Emerg Infect Dis 9:752–753

    Article  PubMed  Google Scholar 

  • Hommez J, Devriese LA, Vaneechoutte M, Riegel P et al (1999) Identification of nonlipophilic corynebacteria isolated form dairy cows with mastitis. J Clin Microbiol 37:954–957

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kamada T, Hatanaka A, Tasaki A, Honda K et al (2012) Case of caused by Corynebacterium ulcerans in Ibaraki Prefecture. Nihon Jibiinkoka Gakkai Kaiho 115:682–686

    Article  PubMed  Google Scholar 

  • Katsukawa C, Kawahara R, Inoue K, Ishii A et al (2009) Toxigenic Corynebacterium ulcerans isolated from the domestic dog for the first time in Japan. Jpn J Infect Dis 62:171–172

    PubMed  Google Scholar 

  • Katsukawa C, Komiya T, Yamagishi H, Ishii A et al (2012) Prevalence of Corynebacterium ulcerans in dogs in Osaka. J Med Microbiol 61:266–273

    Article  PubMed  Google Scholar 

  • Komiya T, Yukiji C, De Zoysa A, Masaaki I et al (2010) Two Japanese Corynebacterium ulcerans isolates from the same hospital: ribotype, toxigenicity and serum antitoxin titre. J Med Microbiol 59:1497–1504

    Article  CAS  PubMed  Google Scholar 

  • Lantz MS, Switalski LM, Kornmam KS, Höök M (1985) Bacteroides intermedius binds fibrinogen. J Bacteriol 163:623–628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lartigue MF, Monnet X, Lê Fleche A, Grimont PA et al (2005) Corynebacterium ulcerans in an immunocompromised patient with diphtheria and her dog. J Clin Microbiol 43:999–1001

    Article  PubMed Central  PubMed  Google Scholar 

  • Leek MD, Sivaloganathan S, Devaraj SK, Zamiri I et al (1990) Diphtheria with a rare difference Corynebacterium fatality with associated apoptotic cell death. Histopathology 6(2):187–189

    Google Scholar 

  • Livornese LL, Korzeniowski OM (1992) Pathogenesis of infective endocarditis. In: Kaye D (ed) Infective endocarditis, 2nd edn. Raven Press, New York, pp 19–35

    Google Scholar 

  • Martınez-Martınez L, Ortega MC, Suarez AL (1995) Comparison of E-test with broth microdilution and disk diffusion for susceptibility testing of coryneform bacteria. J Clin Microbiol 33:1318–1321

    PubMed Central  PubMed  Google Scholar 

  • Mattos-Guaraldi AL, Sampaio JLM, Santos CS, Pimenta FP et al (2008a) First detection of Corynebacterium ulcerans producing diphtheria-like toxin in a case of human with pulmonary infection in the Rio de Janeiro metropolitan area, Brazil. Mem Inst Oswaldo Cruz 103:396–400

    Article  CAS  PubMed  Google Scholar 

  • Mattos-Guaraldi AL, Villas-Boas MHS, Dias AASO, Silva Jr FC et al (2008b) Corynebacterium ulcerans infecting humans and dogs in the metropolitan area of Rio de Janeiro, Brazil. Presented at the proceedings of the second annual meeting of DIPNET & tenth international meeting of the European Laboratory Working Group on Diphtheria, Larnaca, Cyprus, 61

  • Mosesson MW (2005) Fibrinogen and fibrin structure and functions. J Thromb Haemost 3:1894–1904

    Article  CAS  PubMed  Google Scholar 

  • Mosher DF (1975) Cross-linking of cold-insoluble globulin by fibrin-stabilizing factor. J Biol Chem 250:6614–6621

    CAS  PubMed  Google Scholar 

  • Pereira A, Pimenta FP, Santos FRW, Damasco PV et al (2008) Antimicrobial resistance among Brazilian Corynebacterium diphtheriae strains. Mem Inst Oswaldo Cruz 103:507–510

    Article  CAS  PubMed  Google Scholar 

  • Perkins SL, Cordery R, Nixon G, Abrahams A et al (2010) Investigations and control measures following a non-travel-associated case of toxigenic Corynebacterium diphtheriae, London, United Kingdom, December 2009–January 2010. Euro Surveill 15(16),19544

  • Pickering LK, Baker CJ, Kimberlin DW, Long SS (2009) Diphtheria. Red book: 2009 report of the committee on infectious diseases, 28th edn. American Academy of Pediatrics, Elk Grove Village, pp 280–283

    Google Scholar 

  • Pierno M, Maravigna L, Piazza R, Visai L, Speziale P (2006) FbsA-driven fibrinogen polymerization: a bacterial “deceiving strategy”. Phys Rev Lett 96(2):028108. doi:10.1103/PhysRevLett.96.028108

    Google Scholar 

  • Pimenta FP, Souza MC, Pereira GA, Hirata R Jr et al (2008) DNase test as a novel approach for the routine screening of Corynebacterium diphtheriae. Lett Appl Microbiol 46:307–311

    Article  CAS  PubMed  Google Scholar 

  • Puliti M, Hunolstein CV, Marangi M, Bistoni F et al (2006) Experimental model of infection with nontoxigenic strains of Corynebacterium diphtheriae and development of septic arthritis. J Med Microbiol 55:229–235

    Article  CAS  PubMed  Google Scholar 

  • Rennermalm A, Nilsson M, Flock JI (2004) The fibrinogen binding protein of Staphylococcus epidermidis is a target for opsonic antibodies. Infect Immun 72:3081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rivera J, Vannakambadi G, Höök M, Speziale P (2007) Fibrinogen-binding proteins of Gram-positive bacteria. Thromb Haemost 98:503–511

    CAS  PubMed  Google Scholar 

  • Ruoslahti E, Vaheri A (1975) Interaction of soluble fibroblast surface antigen with fibrinogen and fibrin. Identity with cold insoluble globulin of human plasma. J Exp Med 141:497–501

    Article  CAS  PubMed  Google Scholar 

  • Sabbadini PS, Genovez MR, Silva CF, Adelino TL et al (2010) Fibrinogen binds to nontoxigenic and toxigenic Corynebacterium diphtheriae strains. Mem Inst Oswaldo Cruz 105:706–711

    Article  CAS  PubMed  Google Scholar 

  • Schmiel DH, Miller VJ (1999) Bacterial phospholipases and pathogenesis. Microbes Infect 1:1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Schubert A, Zakikhany K, Schreiner M, Frank R et al (2002) A fibrinogen receptor from group B Streptococcus interacts with fibrinogen by repetitive units novel ligand binding sites. Mol Microbiol 46:557–569

    Article  CAS  PubMed  Google Scholar 

  • Sekizuka T, Yamamoto A, Komiya T, Kenri T et al (2012) Corynebacterium ulcerans 0102 carries the gene encoding diphtheria toxin on a prophage different from the C. diphtheriae NCTC 13129 prophage. BMC Microbiol 12:72. doi:10.1186/1471-2180-12-72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun H (2006) The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 21:281–288

    Article  CAS  Google Scholar 

  • Taylor J, Saveedra-Campos M, Harwood D, Pritchard G et al (2010) Toxigenic Corynebacterium ulcerans infection in a veterinary student in London, United Kingdon. Euro Surveill 15:1–3

    Google Scholar 

  • Tenover FC, Arbeit RD, Goering RV, Mickelsen PA et al (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tissi L, Puliti M, Barluzzi R, Orefici G et al (1999) Role of tumor necrosis factor alpha, interleukin-1b, and interleukin-6 in a mouse model of group B streptococcal arthritis. Infect Immun 67:4545–4550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Torres LFC, Ribeiro D, Hirata R Jr, Pacheco LG et al (2013) Multiplex PCR for identification and toxigenicity of Corynebacterium group of zoonotic potential and an overview of human and animal infections. Mem Inst Oswaldo Cruz 108(3):272–279

    CAS  Google Scholar 

  • Trost E, Al-Dilaimi A, Papavasiliou P, Schneider J et al (2011) Comparative analysis of two complete Corynebacterium ulcerans genomes and detection of candidate virulence factors. BMC Genomics 12:383. doi:10.1186/1471-2164-12-383

    Article  PubMed Central  PubMed  Google Scholar 

  • Urakawa T, Seto J, Yamamoto A, Nakajima T et al (2013) (2013) Subcutaneous abscess formation in the upper extremity caused by toxigenic Corynebacterium ulcerans. J Med Microbiol 62:489–493

    Article  PubMed  Google Scholar 

  • Wagner KS, White JM, Neal S, Crowcroft NS et al (2010) Diphtheria in the United Kingdom, 1986–2008: the increasing role of Corynebacterium ulcerans. Epidemiol Infect 138:1519–1530

    Article  CAS  PubMed  Google Scholar 

  • Wellinghausen N, Sing A, Kern WV, Perner S et al (2002) A fatal case of necrotizing sinusitis due to toxigenic Corynebacterium ulcerans. Int J Med Microbiol 292:59–63

    Article  PubMed  Google Scholar 

  • Zakikhany K, Efstratiou A (2012) Diphtheria in Europe: current problems and new challenges. Future Microbiol 7:595–607

    Article  PubMed  Google Scholar 

  • Zamiri I, McEntegar MGT (1972) The sensitivity of diphtheria bacilli to eight antibiotics. J Clin Path 25:716–717

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Programa Estratégico de Apoio à Pesquisa em Saúde-Fundação Oswaldo Cruz (PAPES V-FIOCRUZ), Sub-Reitoria de Pós-graduação e Pesquisa da Universidade do Estado do Rio de Janeiro (SR-2/UERJ).

Conflict of interest

The authors declare that they no have conflict of interest.

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Authors and Affiliations

  1. Laboratory of Diphtheria and Corynebacteria of Clinical Relevance-LDCIC, Collaborating Center for Diphtheria of CGLAB/SVS/MS, School of Medical Sciences, Universidade do Estado do Rio de Janeiro—UERJ, Rio de Janeiro, RJ, Brazil

    Liliane Simpson-Louredo, Juliana Nunes Ramos, Louisy Sanches Santos, Cintia Silva Santos, Raphael Hirata Jr. & Ana Luíza Mattos-Guaraldi

  2. Institute of Microbiology Professor Paulo de Góes, Universidade Federal do Rio de Janeiro (IMPPG/UFRJ), Rio de Janeiro, RJ, Brazil

    Renata Stavracakis Peixoto

  3. Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

    Camila Azevedo Antunes

  4. National Institute for Quality Control in Health (INCQS), Fundação Oswaldo Cruz—FIOCRUZ, Rio de Janeiro, RJ, Brazil

    Liliane Simpson-Louredo, Juliana Nunes Ramos, Elisa Martins Ladeira, Veronica Viana Vieira & Maria Helena Simões Villas Bôas

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  1. Liliane Simpson-Louredo
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  2. Juliana Nunes Ramos
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  3. Renata Stavracakis Peixoto
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  4. Louisy Sanches Santos
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  5. Camila Azevedo Antunes
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  9. Maria Helena Simões Villas Bôas
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  10. Raphael Hirata Jr.
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  11. Ana Luíza Mattos-Guaraldi
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Corresponding author

Correspondence to Ana Luíza Mattos-Guaraldi.

Additional information

L. Simpson-Louredo and J. N. Ramos contributed equally for the first authorship in this manuscript.

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Simpson-Louredo, L., Ramos, J.N., Peixoto, R.S. et al. Corynebacterium ulcerans isolates from humans and dogs: fibrinogen, fibronectin and collagen-binding, antimicrobial and PFGE profiles. Antonie van Leeuwenhoek 105, 343–352 (2014). https://doi.org/10.1007/s10482-013-0080-5

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