Review
Staphylococcus aureus determinants for nasal colonization

https://doi.org/10.1016/j.tim.2012.03.004Get rights and content

Approximately 20% of the healthy human population is persistently colonized in the nasal cavity with Staphylococcus aureus, which constitutes a major risk for infection. S. aureus seems to predominantly colonize the anterior part of the nasal cavity by adhering to nasal surface structures and escaping the host innate and adaptive immune responses. Several bacterial and host factors that play a role in these processes have been identified in the past few years and were in part functionally evaluated in appropriate colonization models. However, the dynamics of host–pathogen crosstalk is only partially understood.

Section snippets

The nasal cavity is the primary habitat of Staphylococcus aureus

Staphylococcus aureus is seen as a commensal as well as a major human pathogen responsible for a wide range of serious acute and chronic diseases. Analysis of isolates from infected patients showed that at least nosocomial infections are mostly endogenous 1, 2 and nasal carriage has been identified as a major risk factor for several types of infections 3, 4, 5. Only approximately 20% of the healthy human population is persistently colonized in the nose with S. aureus. In this group of

S. aureus adherence to nasal surfaces

A crucial step in the establishment of nasal colonization is most likely the adhesion of bacteria to the nasal epithelial cells. S. aureus seems to predominantly colonize the anterior part of the nasal cavity (vestibulum nasi), which is lined by a stratified, keratinized, non-ciliated squamous epithelium. During differentiation, nasal epithelial cells in the anterior change their appearance from columnar to anucleated, squamous cells termed corneocytes, which are highly keratinized and are

Growth conditions and regulatory changes in response to the nasal environment

S. aureus is constantly removed from the nose through shedding of squamous epithelial cells and mucus. Thus, the bacterial proliferation rate has to be high enough to compensate for this mechanical clearance and presumably also other antibacterial defense mechanisms. However, the physiological state of S. aureus in the nasal cavity is not well investigated. Expression analysis of genes that are indicative for certain metabolic states of S. aureus was chosen to address this question 36, 44, 45.

S. aureus immune evasion during colonization

In addition to overcoming the mechanical clearance in the nasal cavity, S. aureus must circumvent innate antibacterial defenses to achieve persistent colonization 49, 50. S. aureus is able to counteract the most important mechanisms, namely antimicrobial molecules such as lysozyme, bactericidal fatty acids, defensins, immunoglobulins and the complement system (Table 2).

S. aureus is lysozyme-resistant due to the combined activity of the cell wall modifying enzyme OatA and the presence of WTA [51]

Concluding remarks

Since the last review on staphylococcal nasal carriage in this journal, a decade ago [5], major progress has been made in understanding the usually well balanced interaction between S. aureus and its host. A large plethora of well conducted genetic studies now convincingly show that almost all S. aureus isolates of human origin can be assigned to a limited number of clonal complexes, all of which are equally efficient in colonizing the human nose. By contrast, human genetic factors seem to be

Acknowledgments

This work was supported by DFG SFB 766 (Weidenmaier, Wolz), DFG SFB TR34 (Weidenmaier, Wolz), and Fortuene Grant 1846-0-0 from the Medical Faculty of the University of Tuebingen (Weidenmaier).

References (80)

  • S.R. Clarke

    The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin

    Cell Host Microbe

    (2007)
  • S.H. Rooijakkers

    Anti-opsonic properties of staphylokinase

    Microbes Infect.

    (2005)
  • S.H. Rooijakkers

    Staphylococcal innate immune evasion

    Trends Microbiol.

    (2005)
  • M. Dall’Antonia

    Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares

    J. Hosp. Infect.

    (2005)
  • D. Bogaert

    Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children

    Lancet

    (2004)
  • Y. Uehara

    Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp

    J. Hosp. Infect.

    (2000)
  • C. von Eiff

    Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group

    N. Engl. J. Med.

    (2001)
  • J.A. Kluytmans et al.

    Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections

    Infection

    (2005)
  • O. Sakwinska

    Ecological temporal stability of Staphylococcus aureus nasal carriage

    J. Clin. Microbiol.

    (2010)
  • C. Goerke

    Molecular epidemiology of community-acquired Staphylococcus aureus in families with and without cystic fibrosis patients

    J. Infect. Dis.

    (2000)
  • A. van Belkum

    Reclassification of Staphylococcus aureus nasal carriage types

    J. Infect. Dis.

    (2009)
  • E.L. van den Akker

    Staphylococcus aureus nasal carriage is associated with glucocorticoid receptor gene polymorphisms

    J. Infect. Dis.

    (2006)
  • M. Emonts

    Host polymorphisms in interleukin 4, complement factor H, and C-reactive protein associated with nasal carriage of Staphylococcus aureus and occurrence of boils

    J. Infect. Dis.

    (2008)
  • R. Ruimy

    Are host genetics the predominant determinant of persistent nasal Staphylococcus aureus carriage in humans?

    J. Infect. Dis.

    (2010)
  • K. Sivaraman

    Staphylococcus aureus nasal carriage and its contributing factors

    Future Microbiol.

    (2009)
  • D.C. Melles

    Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus

    J. Clin. Invest.

    (2004)
  • J.A. Lindsay et al.

    Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus

    Funct. Integr. Genomics

    (2006)
  • P. Zanger

    Import and spread of Panton-Valentine Leukocidin-positive Staphylococcus aureus through nasal carriage and skin infections in travelers returning from the tropics and subtropics

    Clin. Infect. Dis.

    (2012)
  • C. Goerke

    Diversity of prophages in dominant Staphylococcus aureus clonal lineages

    J. Bacteriol.

    (2009)
  • I. Plouin-Gaudon

    Intracellular residency is frequently associated with recurrent Staphylococcus aureus rhinosinusitis

    Rhinology

    (2006)
  • S. Clement

    Evidence of an intracellular reservoir in the nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis

    J. Infect. Dis.

    (2005)
  • C. Weidenmaier et al.

    Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions

    Nat. Rev. Microbiol.

    (2008)
  • P. Speziale

    Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host

    Future Microbiol.

    (2009)
  • L.M. O’Brien

    Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization

    Cell Microbiol.

    (2002)
  • T.J. Foster

    Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion

    Vet. Dermatol.

    (2009)
  • V.K. Ganesh

    A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics

    PLoS Pathog.

    (2008)
  • A.C. Steven et al.

    Protein composition of cornified cell envelopes of epidermal keratinocytes

    J. Cell Sci.

    (1994)
  • S.R. Clarke

    Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins

    Infect. Immun.

    (2009)
  • S.R. Clarke

    Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage

    J. Infect. Dis.

    (2006)
  • R.M. Corrigan

    Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells

    BMC Microbiol.

    (2009)
  • Cited by (118)

    • Staphylococcus aureus

      2023, Molecular Medical Microbiology, Third Edition
    • Ciprofloxacin loaded o/w microemulsion against Staphylococcus aureus. Analytical and biological studies for topical and intranasal administration

      2020, Journal of Drug Delivery Science and Technology
      Citation Excerpt :

      Staphylococcus aureus is a ubiquitous opportunistic bacterial species that can infect, replicate and persist in vertebrate hosts. Although S. aureus can colonize mucosal surfaces of healthy humans with unnoticeable or mild clinical features, it has the invasive potential to generate diverse life threatening infections thus making this species a worldwide threat to public health [1,2]. In addition to the widespread incidence of methicillin-resistant S. aureus (MRSA) [3], infection control is hampered by the evolution of S. aureus with low level vancomycin resistance [4].

    View all citing articles on Scopus
    *

    Current address: Hain Lifescience GmbH, Hardwiesenstrasse 1, 72147 Nehren, Germany.

    View full text