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Abstract

Purpose. Respiratory tract infections (RTIs) are responsible for over 2.8 million deaths per year worldwide with pathobiont carriage a required precursor to infection. We sought to determine carriage epidemiology for both bacterial and viral respiratory pathogens as part of a large population-based cross-sectional carriage study.

Methodology. Nose self-swab samples were collected in two separate time-points, May to August 2012 (late spring/summer) and February to April 2013 (winter/early spring). The presence of six bacterial species: S. pneumoniae, H. influenzae, M. catarrhalis, S. aureus, P. aeruginosa and N. meningitidis in addition to respiratory syncytial virus, influenza viruses A and B, rhinovirus/enterovirus, coronavirus, parainfluenza viruses 1–3 and adenovirus was determined using culture and PCR methods.

Results/Key findings. Carriage was shown to vary with age, recent RTI and the presence of other species. Spatial structures of microbial communities were more disordered in the 0–4 age group and those with recent RTI. Species frequency distributions were flatter than random expectation in young individuals (X=20.42, P=0.002), indicating spatial clumping of species consistent with facilitative relationships. Deviations from a neutral model of ecological niches were observed in summer samples and from older individuals but not in the winter or younger individuals (0–4 years), suggesting the presence of seasonal and age-dependent niche processes in respiratory community assembly.

Conclusion. The application of epidemiological methods and ecological theory to respiratory tract samples has yielded novel insights into the factors that drive microbial community composition.

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2018-06-21
2024-12-03
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References

  1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380:2095–2128 [View Article][PubMed]
    [Google Scholar]
  2. NICE Respiratory Tract Infections – Antibiotic Prescribing Costing Report London, UK: NHS; 2008
    [Google Scholar]
  3. Weiss-Salz I, Yagupsky P. Asymptomatic Carriage of Respiratory Pathogens: “The Wolf shall Dwell with the Lamb…and a Little Child shall Lead them” (Isaiah 11: 6). Open Infect Dis J 2010; 4:11–15 [View Article]
    [Google Scholar]
  4. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013; 9:e1003057 [View Article][PubMed]
    [Google Scholar]
  5. Hubbell SP. The Unified Theory of Biodiversity and Biogeography Priceton, USA: Princeton University Press; 2001
    [Google Scholar]
  6. Tuttle MS, Mostow E, Mukherjee P, Hu FZ, Melton-Kreft R et al. Characterization of bacterial communities in venous insufficiency wounds by use of conventional culture and molecular diagnostic methods. J Clin Microbiol 2011; 49:3812–3819 [View Article][PubMed]
    [Google Scholar]
  7. Dollhopf SL, Hashsham SA, Tiedje JM. Interpreting 16S rDNA T-RFLP Data: application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microb Ecol 2001; 42:495–505 [View Article][PubMed]
    [Google Scholar]
  8. Mackay IM. Real-time PCR in the microbiology laboratory. Clin Microbiol Infect 2004; 10:190–212 [View Article][PubMed]
    [Google Scholar]
  9. Pai R, Gertz RE, Beall B. Sequential multiplex PCR approach for determining capsular serotypes of Streptococcus pneumoniae isolates. J Clin Microbiol 2006; 44:124–131 [View Article][PubMed]
    [Google Scholar]
  10. LaClaire LL, Tondella ML, Beall DS, Noble CA, Raghunathan PL et al. Identification of Haemophilus influenzae serotypes by standard slide agglutination serotyping and PCR-based capsule typing. J Clin Microbiol 2003; 41:393–396 [View Article][PubMed]
    [Google Scholar]
  11. Mothershed EA, Sacchi CT, Whitney AM, Barnett GA, Ajello GW et al. Use of real-time PCR to resolve slide agglutination discrepancies in serogroup identification of Neisseria meningitidis. J Clin Microbiol 2004; 42:320–328 [View Article][PubMed]
    [Google Scholar]
  12. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 1998; 95:3140–3145 [View Article][PubMed]
    [Google Scholar]
  13. Sheppard SK, Jolley KA, Maiden MC. A gene-by-gene approach to bacterial population genomics: whole genome MLST of campylobacter. Genes 2012; 3:261–277 [View Article][PubMed]
    [Google Scholar]
  14. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015 [View Article][PubMed]
    [Google Scholar]
  15. Doncaster CP. Ecological equivalence: a realistic assumption for niche theory as a testable alternative to neutral theory. PLoS One 2009; 4:e7460 [View Article][PubMed]
    [Google Scholar]
  16. Elton CS. Ecological methods. In Huxley JS. (editor) Animal Ecology London, UK: Sidgwick & Jackson Limited; 1927 pp. 207
    [Google Scholar]
  17. Schoener TW. Resource partitioning in ecological communities. Science 1974; 185:27–39 [View Article][PubMed]
    [Google Scholar]
  18. McGill BJ. A test of the unified neutral theory of biodiversity. Nature 2003; 422:881–885 [View Article][PubMed]
    [Google Scholar]
  19. Southwood TRE. The number of species of insect associated with various trees. J Anim Ecol 1961; 30:1–8 [View Article]
    [Google Scholar]
  20. Verbruggen E, van der Heijden MG, Weedon JT, Kowalchuk GA, Röling WF. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 2012; 21:2341–2353 [View Article][PubMed]
    [Google Scholar]
  21. Rohde K, Worthen WB, Heap M, Hugueny B, Guégan JF. Nestedness in assemblages of metazoan ecto- and endoparasites of marine fish. Int J Parasitol 1998; 28:543–549 [View Article][PubMed]
    [Google Scholar]
  22. Coughtrie AL, Whittaker RN, Begum N, Anderson R, Tuck A et al. Evaluation of swabbing methods for estimating the prevalence of bacterial carriage in the upper respiratory tract: a cross sectional study. BMJ Open 2014; 4:e005341 [View Article][PubMed]
    [Google Scholar]
  23. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article][PubMed]
    [Google Scholar]
  24. R: A Language and Environment for Statistical Computing. Vienna, Austria: 2017
    [Google Scholar]
  25. MacArthur RH. On the relative abundance of bird species. Proc Natl Acad Sci USA 1957; 43:293–295 [View Article][PubMed]
    [Google Scholar]
  26. King CE. Relative abundance of species and MacArthur's model. Ecology 1964; 45:716–727 [View Article]
    [Google Scholar]
  27. Tocheva AS, Jefferies JM, Rubery H, Bennett J, Afimeke G et al. Declining serotype coverage of new pneumococcal conjugate vaccines relating to the carriage of Streptococcus pneumoniae in young children. Vaccine 2011; 29:4400–4404 [View Article][PubMed]
    [Google Scholar]
  28. Miller E, Andrews NJ, Waight PA, Slack MP, George RC. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect Dis 2011; 11:760–768 [View Article][PubMed]
    [Google Scholar]
  29. Hanage WP, Finkelstein JA, Huang SS, Pelton SI, Stevenson AE et al. Evidence that pneumococcal serotype replacement in Massachusetts following conjugate vaccination is now complete. Epidemics 2010; 2:80–84 [View Article][PubMed]
    [Google Scholar]
  30. Feikin DR, Kagucia EW, Loo JD, Link-Gelles R, Puhan MA et al. Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites. PLoS Med 2013; 10:e1001517 [View Article][PubMed]
    [Google Scholar]
  31. Jeraldo P, Sipos M, Chia N, Brulc JM, Dhillon AS et al. Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc Natl Acad Sci USA 2012; 109:9692–9698 [View Article][PubMed]
    [Google Scholar]
  32. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 2010; 4:337–345 [View Article][PubMed]
    [Google Scholar]
  33. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI et al. Bacterial community variation in human body habitats across space and time. Science 2009; 326:1694–1697 [View Article][PubMed]
    [Google Scholar]
  34. Cobey S, Lipsitch M. Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science 2012; 335:1376–1380 [View Article][PubMed]
    [Google Scholar]
  35. Mikkelson GM. Ecological niches: linking classical and contemporary approaches. Biol Philos 2005; 20:557–566
    [Google Scholar]
  36. Chase JM, Leibold MA. Ecological Niches: Linking Classical and Contemporary Approaches Chicago, USA: University of Chicago Press; 2003
    [Google Scholar]
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