The ecology of nasal colonization of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus: the role of competition and interactions with host's immune response

Abstract

BackgroundThe first step in invasive disease caused by the normally commensal bacteria Streptococcus pneumoniae, Staphylococcus aureus and Haemophilus influenzae is their colonization of the nasal passages. For any population to colonize a new habitat it is necessary for it to be able to compete with the existing organisms and evade predation. In the case of colonization of these species the competition is between strains of the same and different species of bacteria and the predation is mediated by the host's immune response. Here, we use a neonatal rat model to explore these elements of the ecology of nasal colonization by these occasionally invasive bacteria.ResultsWhen neonatal rats are colonized by any one of these species the density of bacteria in the nasal passage rapidly reaches a steady-state density that is species-specific but independent of inoculum size. When novel populations of H. influenzae and S. pneumoniae are introduced into the nasal passages of neonatal rats with established populations of the same species, residents and invaders coexisted. However, this was not the case for S. aureus - the established population inhibited invasion of new S. aureus populations. In mixed-species introductions, S. aureus or S. pneumoniae facilitated the invasion of another H. influenzae population; for other pairs the interaction was antagonistic and immune-mediated. For example, under some conditions H. influenzae promoted an immune response which limited the invasion of S. pneumoniae.ConclusionsNasal colonization is a dynamic process with turnover of new strains and new species. These results suggest that multiple strains of either H. influenzae or S. pneumoniae can coexist; in contrast, S. aureus strains require a host to have no other S. aureus present to colonize. Levels of colonization (and hence the possible risk of invasive disease) by H. influenzae are increased in hosts pre-colonized with either S. aureus or S. pneumoniae.

Culture and molecular-based profiles show shifts in bacterial communities of the upper respiratory tract that occur with age

“…The microbiota is involved in resistance to colonization by incoming pathogens (Kelley et al, 2005;Margolis et al, 2010), education of the immune system (Lathrop et al, 2011) and regulation of host immunocompetence in the lung in response to infection (Ichinohe et al, 2011).…”

Staphylococcus aureusandStreptococcus pneumoniaeinteraction and response to pneumococcal vaccination: Myth or reality?

“…5,8,[33][34][35][36][37] Positive correlations between S. pneumoniae, M. catarrhalis and H. influenza, and negative correlations between H. influenza and S. aureus have been reported in epidemiological studies 5,7,8,38,39 as well as infection models. 40,25,41 Pettigrew et al showed that colonization with M. catarrhalis and H. influenza together doubled the likelihood of co-colonization with S. pneumoniae.…”

“…Over the years, many studies have observed interactions between various bacterial species and viruses carried in the upper respiratory tract. [26][27][28][29][30] These bacteria and viruses compete for space and resources 25,30,31 and in some cases, such as influenza virus and S. pneumoniae, the virus and bacteria act synergistically to cause increased S. pneumoniae adhesion to host cells. 32 The most clinically relevant and commonly studied interactions and competition are those between the upper respiratory tract pathogens, namely S. pneumoniae, S. aureus, H influenzae, and M. catarrhalis.…”

“…24 Margolis et al determined that the colonizing strain of S. aureus in a neonatal rat model is determined solely by which strain is first to colonize and not by the characteristics of that strain. 25 Interactions with other residents of the upper respiratory tract microbiome S. aureus and S. pneumoniae are not the only species present in the nasopharyngeal region. Over the years, many studies have observed interactions between various bacterial species and viruses carried in the upper respiratory tract.…”

Viral/bacterial respiratory tract co-infections in children

“…However, none of these trends were statistically significant, and no clear associations were observed between S. pneumoniae influenzae from complement-mediated killing (283). S. pneumoniae colonisation has been shown to increase H. influenzae density in the nasopharynx of neonatal rats (280). However, the same study found that H. influenzae colonisation reduced S. pneumoniae density (280), and another study in a murine model has demonstrated complement-dependent phagocytosis of S. pneumoniae induced by co-colonisation with H. influenzae (279).…”