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Even though our data suggested nonencapsulated pneumococci were more quickly cleared from the conjunctiva, most reported outbreaks of pneumococcal conjunctivitis were caused by nonencapsulated strains. It is well established that pneumococcal capsule has the ability to mask pneumococcal adhesins and that nonencapsulated pneumococci may have an advantage in colonization by allowing the exposure of important surface proteins.
However, these same bacteria had significant reduction in their virulence in an intravenous infection model. Our data underscore that the eye is a unique site of infection for pneumococci. Results observed for keratitis and conjunctivitis are in stark contrast to all other pneumococcal infections in which capsule is necessary to cause pathology. In the cornea and conjunctiva, the main virulence factors are non-capsular components.
This important difference in the basic mechanism of pneumococcal infection should be considered in analyses of pneumococcal virulence such that generalizations are not made for all host infection sites. Previous work by Williamson et al. Using microarray analysis, they showed that nonencapsulated conjunctivitis isolates upregulated the expression of neuraminidases in vitro. Furthermore, these isolates had reduced binding to human conjunctival epithelial cells that expressed high levels of mucin compared to conjunctival epithelial cells that expressed low levels of mucin.
Moreover, this reduced binding was enhanced with the addition of exogenous neuraminidases. The authors proposed that mucin may act as a barrier to pneumococcal binding at the ocular surface but that the upregulation of neuraminidases in conjunctivitis isolates may contribute to the adherence of the bacterium to the conjunctival surface by degrading host mucin in vivo.
This previous study, however, only examined the in vitro effect of neuraminidases and mucin on the binding and invasion abilities of nonencapsulated conjunctivitis isolates.
While the presence of neuraminidases may affect binding and invasion in vitro , the importance of neuraminidases in vivo often depends on the host tissue and location of the infection. Likewise, host immune responses cannot fully be examined in cultured conjunctival cells.
The effect of NanA on virulence has been studied in a variety of model systems with mixed results. Our study used an isogenic capsule mutant and parent and an in vivo approach to better elucidate the role of pneumococcal capsule and neuraminidase production in the conjunctiva. The nonencapsulated strain had similar neuraminidase activity compared to the parent strain when grown in vitro ; however, had significantly greater activity than the parent following conjunctival infection in the rabbit.
Interestingly, the neuraminidase activity of the parent strain after infection in vivo was significantly less than the activity after growth in vitro , whereas the neuraminidase activity of the mutant strain after infection was significantly more than after growth in vitro Figure 5.
Because only the bacterial pellet was assayed for neuraminidase activity, we believe that the increased activity seen in vivo can be attributed solely to NanA, as NanA is the only pneumococcal neuraminidase which contains the C-terminal cell surface anchorage domain and, therefore, is the only neuraminidase found in the bacterial pellet. Most research regarding pneumococcal NanA expression is performed on encapsulated pneumococci, probably because in most infections types, capsule is required for pathology.
In the conjunctivae, the nonencapsulated strain was cleared more rapidly although it possessed significantly higher NanA activity than the encapsulated strain. It is possible that the model system used injected bacteria versus topically applied bacteria fails to fully account for the role of NanA, which we hypothesize to be important in the initial binding of the bacteria.
It is possible that in the conjunctivae, where capsule is unimportant to disease severity, a nonencapsulated strain may have some kind of selective advantage that allows it to increase NanA production, thus allowing the bacteria to utilize ocular mucins as a carbon source. This would permit the pneumococci to reach higher levels of growth at the conjunctival surface and possibly allow for more opportunities to invade the conjunctival epithelium and, thus, establish an infection.
Another possible explanation for the increase in neuraminidase activity observed in the nonencapsulated strain may be that the lack of capsule exposes a receptor that when stimulated by some host factor causes the bacterium to increase its neuraminidase production. Our preliminary in vivo data combined with the in vitro data from Williamson et al.
Additional studies in vivo are underway to better elucidate this role. Additional bacterial receptors may play a significant role in the initial binding of nonencapsulated pneumococci to conjunctival epithelial cells. Pneumococcal adherence to epithelial cells, including conjunctival epithelial cells, was shown to be reduced in bacteria not expressing a recently described receptor, plasminogen- and fibronectin-binding protein B PfbB.
Bacterial adherence to epithelial cells was reduced in both encapsulated and nonencapsulated strains that lacked PfbB. Our data underscores the idea that isolation of noncapsular strains in conjunctivitis could be due to an initial binding event since our model cannot yet accommodate a topical infection. This loss of capsule could hypothetically be due to an unknown down-regulation of capsule biosynthesis locus genes in response to an environmental signal.
This hypothesis was tested using the Pneumoslide kit in which the presence of the bacterial capsule was confirmed prior to infection and then assessed again on bacteria recovered from the conjunctivae at 3 and 12 hr post-infection. Our results showed that capsule production was unaffected in vivo and bacteria recovered from conjunctivae infected with an encapsulated strain continued to produce capsule.
This indicates that the predominance of nonencapsulated pneumococci found in conjunctivitis may be due to an initial binding step. However, this capsule assay simply assessed presence or absence and failed to take into account the amount of capsule produced. Moreover, the use of specific pathogen-free animals might have affected the outcome as interactions between pneumococci and normal ocular flora that may contribute to variations in capsule production were missing.
The presence of capsule has little effect on the severity of pneumococcal conjunctivitis; however, not much is known about additional pneumococcal virulence factors that may be at play. Pneumolysin, a cholesterol dependent cytotoxin, is a known virulence factor associated with systemic as well as ocular infections. Johnson et al. This influx of PMNs may be, at least in part, due to pneumolysin though it could be also be due to other factors or a combination of other factors and pneumolysin.
Further study needs to ascertain the importance of pneumolysin to this infection and possibly address the effectiveness of therapies aimed at the toxin. In conclusion, the present study demonstrates the varied role of capsule in ocular infections. While its presence does not affect the pathology or amount of bacteria recovered after a keratitis infection, the absence of capsule causes a reduction in the number of bacteria recovered from an infected conjunctiva.
Additionally, the nonencapsulated pneumococci had increased neuraminidase activity levels in vivo when compared to the parent strain.
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