1887

Abstract

The colonization dynamics of were studied in a population comprising 1079 healthy children living in Rotterdam, The Netherlands (the Generation R Focus cohort). A total of 2751 nasal swabs were obtained during four clinic visits timed to take place at 1.5, 6, 14 and 24 months of age, yielding a total of 709 and 621 isolates. Between January 2004 and December 2006, approximate but regular 6-monthly cycles of colonization were observed, with peak colonization incidences occurring in the autumn/winter for , and winter/spring for . Co-colonization was significantly more likely than single-species colonization with either or , with genotypic analysis revealing no clonality for co-colonizing or single colonizers of either bacterial species. This finding is especially relevant considering the recent discovery of the importance of quorum sensing in biofilm formation and host clearance. Bacterial genotype heterogeneity was maintained over the 3-year period of the study, even within this relatively localized geographical region, and there was no association of genotypes with either season or year of isolation. Furthermore, chronological and genotypic diversity in three immunologically important virulence genes (, and ) was also observed. This study indicates that genotypic variation is a key factor contributing to the success of colonization of healthy children in the first years of life. Furthermore, variation in immunologically relevant virulence genes within colonizing populations, and even within genotypically identical isolates, may be a result of immune evasion by this pathogen. Finally, the factors facilitating and co-colonization need to be further investigated.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.042929-0
2011-01-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/1/169.html?itemId=/content/journal/micro/10.1099/mic.0.042929-0&mimeType=html&fmt=ahah

References

  1. Akimana, C. & Lafontaine, E. R. ( 2007; ). The Moraxella catarrhalis outer membrane protein CD contains two distinct domains specifying adherence to human lung cells. FEMS Microbiol Lett 271, 12–19.[CrossRef]
    [Google Scholar]
  2. Arkema, J. M., Meijer, A., Meerhoff, T. J., Van Der Velden, J. & Paget, W. J. ( 2008; ). Epidemiological and virological assessment of influenza activity in Europe, during the 2006–2007 winter. Euro Surveill 13, 18958.
    [Google Scholar]
  3. Armbruster, C. E., Hong, W., Pang, B., Weimer, K. E., Juneau, R. A., Turner, J. & Swords, W. E. ( 2010; ). Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio 1, e00102–e00110.
    [Google Scholar]
  4. Bakaletz, L. O. ( 1995; ). Viral potentiation of bacterial superinfection of the respiratory tract. Trends Microbiol 3, 110–114.[CrossRef]
    [Google Scholar]
  5. Balder, R., Hassel, J., Lipski, S. & Lafontaine, E. R. ( 2007; ). Moraxella catarrhalis strain O35E expresses two filamentous hemagglutinin-like proteins that mediate adherence to human epithelial cells. Infect Immun 75, 2765–2775.[CrossRef]
    [Google Scholar]
  6. Berner, R., Schumacher, R. F., Brandis, M. & Forster, J. ( 1996; ). Colonization and infection with Moraxella catarrhalis in childhood. Eur J Clin Microbiol Infect Dis 15, 506–509.[CrossRef]
    [Google Scholar]
  7. Bullard, B., Lipski, S. L. & Lafontaine, E. R. ( 2005; ). Hag directly mediates the adherence of Moraxella catarrhalis to human middle ear cells. Infect Immun 73, 5127–5136.[CrossRef]
    [Google Scholar]
  8. Deich, R. A. & Hoyer, L. C. ( 1982; ). Generation and release of DNA-binding vesicles by Haemophilus influenzae during induction and loss of competence. J Bacteriol 152, 855–864.
    [Google Scholar]
  9. Edwards, K. J., Schwingel, J. M., Datta, A. K. & Campagnari, A. A. ( 2005; ). Multiplex PCR assay that identifies the major lipooligosaccharide serotype expressed by Moraxella catarrhalis clinical isolates. J Clin Microbiol 43, 6139–6143.[CrossRef]
    [Google Scholar]
  10. Faden, H., Waz, M. J., Bernstein, J. M., Brodsky, L., Stanievich, J. & Ogra, P. L. ( 1991; ). Nasopharyngeal flora in the first three years of life in normal and otitis-prone children. Ann Otol Rhinol Laryngol 100, 612–615.[CrossRef]
    [Google Scholar]
  11. Faden, H., Duffy, L., Wasielewski, R., Wolf, J., Krystofik, D. & Tung, Y. ( 1997; ). Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville pediatrics. J Infect Dis 175, 1440–1445.[CrossRef]
    [Google Scholar]
  12. Forsgren, A., Brant, M., Mollenkvist, A., Muyombwe, A., Janson, H., Woin, N. & Riesbeck, K. ( 2001; ). Isolation and characterization of a novel IgD-binding protein from Moraxella catarrhalis. J Immunol 167, 2112–2120.[CrossRef]
    [Google Scholar]
  13. Freid, V. M., Makuc, D. M. & Rooks, R. N. ( 1998; ). Ambulatory health care visits by children: principal diagnosis and place of visit. Vital Health Stat 13, 1–23.
    [Google Scholar]
  14. Gonzales, R., Malone, D. C., Maselli, J. H. & Sande, M. A. ( 2001; ). Excessive antibiotic use for acute respiratory infections in the United States. Clin Infect Dis 33, 757–762.[CrossRef]
    [Google Scholar]
  15. Hays, J. P., Eadie, K., Verduin, C. M., Hazelzet, J., Verbrugh, H. & van Belkum, A. ( 2003; ). Changes in genetic types and population dynamics of Moraxella catarrhalis in hospitalized children are not associated with an exacerbation of existing disease. J Med Microbiol 52, 815–820.[CrossRef]
    [Google Scholar]
  16. Helminen, M. E., Maciver, I., Latimer, J. L., Klesney-Tait, J., Cope, L. D., Paris, M., McCracken, G. H., Jr & Hansen, E. J. ( 1994; ). A large, antigenically conserved protein on the surface of Moraxella catarrhalis is a target for protective antibodies. J Infect Dis 170, 867–872.[CrossRef]
    [Google Scholar]
  17. Helminen, M. E., Beach, R., Maciver, I., Jarosik, G., Hansen, E. J. & Leinonen, M. ( 1995; ). Human immune response against outer membrane proteins of Moraxella (Branhamella) catarrhalis determined by immunoblotting and enzyme immunoassay. Clin Diagn Lab Immunol 2, 35–39.
    [Google Scholar]
  18. Hendley, J. O., Hayden, F. G. & Winther, B. ( 2005; ). Weekly point prevalence of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis in the upper airways of normal young children: effect of respiratory illness and season. APMIS 113, 213–220.[CrossRef]
    [Google Scholar]
  19. Hill, D. J. & Virji, M. ( 2003; ). A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol Microbiol 48, 117–129.[CrossRef]
    [Google Scholar]
  20. Hill, D. J., Toleman, M. A., Evans, D. J., Villullas, S., Van Alphen, L. & Virji, M. ( 2001; ). The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol Microbiol 39, 850–862.[CrossRef]
    [Google Scholar]
  21. Hill, D. J., Edwards, A. M., Rowe, H. A. & Virji, M. ( 2005; ). Carcinoembryonic antigen-related cell adhesion molecule (CEACAM)-binding recombinant polypeptide confers protection against infection by respiratory and urogenital pathogens. Mol Microbiol 55, 1515–1527.[CrossRef]
    [Google Scholar]
  22. Jaddoe, V. W., Bakker, R., van Duijn, C. M., van der Heijden, A. J., Lindemans, J., Mackenbach, J. P., Moll, H. A., Steegers, E. A., Tiemeier, H. & other authors ( 2007; ). The Generation R Study Biobank: a resource for epidemiological studies in children and their parents. Eur J Epidemiol 22, 917–923.[CrossRef]
    [Google Scholar]
  23. Jaddoe, V. W., van Duijn, C. M., van der Heijden, A. J., Mackenbach, J. P., Moll, H. A., Steegers, E. A., Tiemeier, H., Uitterlinden, A. G., Verhulst, F. C. & Hofman, A. ( 2008; ). The Generation R Study: design and cohort update until the age of 4 years. Eur J Epidemiol 23, 801–811.[CrossRef]
    [Google Scholar]
  24. Konno, M., Baba, S., Mikawa, H., Hara, K., Matsumoto, F., Kaga, K., Nishimura, T., Kobayashi, T., Furuya, N. & other authors ( 2006; ). Study of upper respiratory tract bacterial flora: first report. Variations in upper respiratory tract bacterial flora in patients with acute upper respiratory tract infection and healthy subjects and variations by subject age. J Infect Chemother 12, 83–96.[CrossRef]
    [Google Scholar]
  25. Leibovitz, E. ( 2003; ). Acute otitis media in pediatric medicine: current issues in epidemiology, diagnosis, and management. Paediatr Drugs 5 (Suppl. 1), 1–12.[CrossRef]
    [Google Scholar]
  26. Levy, F., Leman, S. C., Sarubbi, F. A. & Walker, E. S. ( 2009; ). Nosocomial transmission clusters and risk factors in Moraxella catarrhalis. Epidemiol Infect 137, 581–590.[CrossRef]
    [Google Scholar]
  27. Lipski, S. L., Akimana, C., Timpe, J. M., Wooten, R. M. & Lafontaine, E. R. ( 2007; ). The Moraxella catarrhalis autotransporter McaP is a conserved surface protein that mediates adherence to human epithelial cells through its N-terminal passenger domain. Infect Immun 75, 314–324.[CrossRef]
    [Google Scholar]
  28. Liu, D. F., McMichael, J. C. & Baker, S. M. ( 2007; ). Moraxella catarrhalis outer membrane protein CD elicits antibodies that inhibit CD binding to human mucin and enhance pulmonary clearance of M. catarrhalis in a mouse model. Infect Immun 75, 2818–2825.[CrossRef]
    [Google Scholar]
  29. Marchisio, P., Gironi, S., Esposito, S., Schito, G. C., Mannelli, S. & Principi, N. ( 2001; ). Seasonal variations in nasopharyngeal carriage of respiratory pathogens in healthy Italian children attending day-care centres or schools. J Med Microbiol 50, 1095–1099.
    [Google Scholar]
  30. Meier, P. S., Freiburghaus, S., Martin, A., Heiniger, N., Troller, R. & Aebi, C. ( 2003; ). Mucosal immune response to specific outer membrane proteins of Moraxella catarrhalis in young children. Pediatr Infect Dis J 22, 256–262.
    [Google Scholar]
  31. Meijer, A., Meerhoff, T. J., Meuwissen, L. E., van der Velden, J. & Paget, W. J. ( 2007; ). Epidemiological and virological assessment of influenza activity in Europe during the winter 2005–2006. Euro Surveill 12, E11–E12.
    [Google Scholar]
  32. Moor, P. E., Collignon, P. C. & Gilbert, G. L. ( 1999; ). Pulsed-field gel electrophoresis used to investigate genetic diversity of Haemophilus influenzae type b isolates in Australia shows differences between Aboriginal and non-Aboriginal isolates. J Clin Microbiol 37, 1524–1531.
    [Google Scholar]
  33. Murphy, T. F. & Parameswaran, G. I. ( 2009; ). Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 49, 124–131.[CrossRef]
    [Google Scholar]
  34. Peerbooms, P. G., Engelen, M. N., Stokman, D. A., van Benthem, B. H., van Weert, M. L., Bruisten, S. M., van Belkum, A. & Coutinho, R. A. ( 2002; ). Nasopharyngeal carriage of potential bacterial pathogens related to day care attendance, with special reference to the molecular epidemiology of Haemophilus influenzae. J Clin Microbiol 40, 2832–2836.[CrossRef]
    [Google Scholar]
  35. Pettigrew, M. M., Gent, J. F., Revai, K., Patel, J. A. & Chonmaitree, T. ( 2008; ). Microbial interactions during upper respiratory tract infections. Emerg Infect Dis 14, 1584–1591.[CrossRef]
    [Google Scholar]
  36. Pichichero, M. E. ( 2000; ). Short course antibiotic therapy for respiratory infections: a review of the evidence. Pediatr Infect Dis J 19, 929–937.[CrossRef]
    [Google Scholar]
  37. Plasschaert, A. I., Rovers, M. M., Schilder, A. G., Verheij, T. J. & Hak, E. ( 2006; ). Trends in doctor consultations, antibiotic prescription, and specialist referrals for otitis media in children: 1995–2003. Pediatrics 117, 1879–1886.[CrossRef]
    [Google Scholar]
  38. Principi, N., Marchisio, P., Schito, G. C. & Mannelli, S. ( 1999; ). Risk factors for carriage of respiratory pathogens in the nasopharynx of healthy children. Ascanius Project Collaborative Group. Pediatr Infect Dis J 18, 517–523.[CrossRef]
    [Google Scholar]
  39. Riesbeck, K., Tan, T. T. & Forsgren, A. ( 2006; ). MID and UspA1/A2 of the human respiratory pathogen Moraxella catarrhalis, and interactions with the human host as basis for vaccine development. Acta Biochim Pol 53, 445–456.
    [Google Scholar]
  40. Ruckdeschel, E. A., Kirkham, C., Lesse, A. J., Hu, Z. & Murphy, T. F. ( 2008; ). Mining the Moraxella catarrhalis genome: identification of potential vaccine antigens expressed during human infection. Infect Immun 76, 1599–1607.[CrossRef]
    [Google Scholar]
  41. Ruckdeschel, E. A., Brauer, A. L., Johnson, A. & Murphy, T. F. ( 2009; ). Characterization of proteins Msp22 and Msp75 as vaccine antigens of Moraxella catarrhalis. Vaccine 27, 7065–7072.[CrossRef]
    [Google Scholar]
  42. Ruuskanen, O., Arola, M., Heikkinen, T. & Ziegler, T. ( 1991; ). Viruses in acute otitis media: increasing evidence for clinical significance. Pediatr Infect Dis J 10, 425–427.[CrossRef]
    [Google Scholar]
  43. Sarantis, H. & Gray-Owen, S. D. ( 2007; ). The specific innate immune receptor CEACAM3 triggers neutrophil bactericidal activities via a Syk kinase-dependent pathway. Cell Microbiol 9, 2167–2180.[CrossRef]
    [Google Scholar]
  44. Slevogt, H., Zabel, S., Opitz, B., Hocke, A., Eitel, J., N'guessan, P. D., Lucka, L., Riesbeck, K., Zimmermann, W. & other authors ( 2008; ). CEACAM1 inhibits Toll-like receptor 2-triggered antibacterial responses of human pulmonary epithelial cells. Nat Immunol 9, 1270–1278.[CrossRef]
    [Google Scholar]
  45. Tan, T. T., Christensen, J. J., Dziegiel, M. H., Forsgren, A. & Riesbeck, K. ( 2006a; ). Comparison of the serological responses to Moraxella catarrhalis immunoglobulin D-binding outer membrane protein and the ubiquitous surface proteins A1 and A2. Infect Immun 74, 6377–6386.[CrossRef]
    [Google Scholar]
  46. Tan, T. T., Forsgren, A. & Riesbeck, K. ( 2006b; ). The respiratory pathogen Moraxella catarrhalis binds to laminin via ubiquitous surface proteins A1 and A2. J Infect Dis 194, 493–497.[CrossRef]
    [Google Scholar]
  47. Tan, T. T., Morgelin, M., Forsgren, A. & Riesbeck, K. ( 2007; ). Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J Infect Dis 195, 1661–1670.[CrossRef]
    [Google Scholar]
  48. Verduin, C. M., Kools-Sijmons, M., van der Plas, J., Vlooswijk, J., Tromp, M., van Dijk, H., Banks, J., Verbrugh, H. & van Belkum, A. ( 2000; ). Complement-resistant Moraxella catarrhalis forms a genetically distinct lineage within the species. FEMS Microbiol Lett 184, 1–8.[CrossRef]
    [Google Scholar]
  49. Verduin, C. M., Hol, C., Fleer, A., van Dijk, H. & van Belkum, A. ( 2002; ). Moraxella catarrhalis: from emerging to established pathogen. Clin Microbiol Rev 15, 125–144.[CrossRef]
    [Google Scholar]
  50. Verhaegh, S. J., Streefland, A., Dewnarain, J. K., Farrell, D. J., van Belkum, A. & Hays, J. P. ( 2008; ). Age-related genotypic and phenotypic differences in Moraxella catarrhalis isolates from children and adults presenting with respiratory disease in 2001–2002. Microbiology 154, 1178–1184.[CrossRef]
    [Google Scholar]
  51. Verhaegh, S. J., Lebon, A., Saarloos, J. A., Verbrugh, H. A., Jaddoe, V. W., Hofman, A., Hays, J. P., Moll, H. A. & van Belkum, A. ( 2010; ). Determinants of Moraxella catarrhalis colonization in healthy Dutch children during the first 14 months of life. Clin Microbiol Infect 16, 992–997.[CrossRef]
    [Google Scholar]
  52. Vlastarakos, P. V., Nikolopoulos, T. P., Korres, S., Tavoulari, E., Tzagaroulakis, A. & Ferekidis, E. ( 2007; ). Grommets in otitis media with effusion: the most frequent operation in children. But is it associated with significant complications? Eur J Pediatr 166, 385–391.[CrossRef]
    [Google Scholar]
  53. Wolf, B., Kools-Sijmons, M., Verduin, C., Rey, L. C., Gama, A., Roord, J., Verhoef, J. & van Belkum, A. ( 2000; ). Genetic diversity among strains of Moraxella catarrhalis cultured from the nasopharynx of young and healthy Brazilian, Angolan and Dutch children. Eur J Clin Microbiol Infect Dis 19, 759–764.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.042929-0
Loading
/content/journal/micro/10.1099/mic.0.042929-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error