Oropharyngeal and nasal Staphylococcus aureus carriage by healthy children

Staphylococcus aureus carriers are at increased risk of developing S. aureus infections after invasive medical or surgical procedures, and more frequently develop S. aureus bacteremia when admitted to hospital [1]. Consequently, routine admission screening is strongly recommended in high-risk units, and the general screening of all hospitalised patients is debated [2]. The emergence of methicillin-resistant S. aureus (MRSA), and evidence that difficult to treat S. aureus-related diseases can also occur in the community has increased the importance of general screening in order to monitor S. aureus circulation and its susceptibility to antibiotics [3], and also explains why S. aureus carriage in the community has recently been periodically evaluated [4],[5].

S. aureus screening is usually carried out using nasal swabs because the anterior nares are considered the primary site of S. aureus colonisation, which can be found in the nares of up to 40% of healthy subjects [6]. Additional screening is currently considered unnecessary [1], but the findings of recent studies indicate that the throat can also be an important site of S. aureus colonisation, and that a relatively large number of subjects may be colonised exclusively in the throat [7]-[11], and would be missed by nasal screening. This has led some authors to conclude that S. aureus screening should include both nose and throat swabs in order to allow a complete evaluation [12]. Most studies of throat carriage have involved hospitalised adults, and there are very few data concerning children. However, as healthy children are the main reservoir of respiratory pathogens and the main cause of bacterial diffusion in the community [1], it could be interesting to investigate the type of screening that should be used during the early years of life in order to obtain a more precise estimate of S. aureus circulation.

The parents of more than 70 % of the children attending the selected schools agreed to allow their children to take part in the study, but 35 (6.6%) of the 532 potential participants were excluded because of mild upper respiratory tract infections. Of the 497 remaining children, 264 (53.1%) were identified as S. aureus carriers: 129 (25.9%) oropharyngeal carriers and 195 (39.2%) nasal carriers, of whom 60 (12.1%) were both oropharyngeal and nasal carriers. This indicates that the use of oropharyngeal swabs increased the identification of S. aureus carriage by about 13.8%. Table 1 shows the oropharyngeal and/or nasal carriage of S. aureus in the study population by age group and methicillin susceptibility. Oropharyngeal carriage increased with age (p < 0.001), whereas nasal carriage decreased. However, the differences between the age groups were statistically significant only in the case of oropharyngeal carriage. There was little or no agreement between oropharyngeal and nasal carriage in any of the age groups. MRSA was identified in only three cases (0.6%), always in nasal samples.

Table 2 shows the general characteristics of the study population by S. aureus carrier status. There were no differences between the carriers and non-carriers in terms of the distribution of age, gender, ethnicity, the number of siblings in the household, exposure to passive smoking, previous clinical history, allergic sensitisation, or previous influenza, pneumococcal and meningococcal vaccinations.

Table 3 shows the main characteristics of the children carrying S. aureus by site of positivity. The children with positive nasal swabs alone were younger than those with positive oropharyngeal swabs alone (p < 0.001) or positive nasal and oropharyngeal swabs (p = 0.01). The frequency of male children was higher among the subjects with positive oropharyngeal and nasal swabs (66.7%) than among those with positive oropharyngeal swabs alone (46.4%; p = 0.02). There were no statistically significant differences in any of the other considered characteristics.

This first study of oropharyngeal and nasal S. aureus colonisation rates in healthy school children shows that, like adults with a history of exposure to the healthcare system [7]-[11], they frequently carry S. aureus in the throat and that this may occur even in the absence of nasal colonisation in a relatively high proportion of cases. Although oropharyngeal sampling led to the detection of S. aureus carriage in fewer children than nasal sampling, it did identify about 14% of children who would have been considered negative on the basis of a nasal swab alone. The global carriage rate of more than 53% was similar to that observed in adults who have provided both nasal and oropharyngeal samples [7]-[11], but significantly higher than that reported in healthy children who have undergone nasal evaluation alone [1], thus highlighting the importance of throat sampling. In this study S. aureus was identified by PCR assay and not by culture. Consequently, genotyping or phenotyping data of the pathogen cannot be presented and it was not possible to establish whether more than one strain type of S. aureus could be identified in children carrying this pathogen. However, molecular techniques used in this study can be adequate for an easier and faster epidemiological evaluation of S. aureus carriage in the general pediatric population in order to have useful information concerning the circulation of MRSA in the community and the risk of the occurrence of community acquired (CA)-S. aureus illnesses that are potentially difficult to treat. The very limited circulation of MRSA found in this study could be, at least in part, due to the enrolment of children who did not receive any antibiotic treatment in the previous three weeks and for whom no antibiotic selection of oropharyngeal flora favouring MRSA emergence occurred. However, the finding suggests a marginal risk of CA disease due to MRSA in Milan: however, it is worth remembering that, although such diseases are relatively uncommon among the general population of Europe, they are considerably more frequent in intensive care units and hospital wards caring for patients with chronic diseases [14]-[16].

The fact that the rates of exclusively oropharyngeal carriage were significantly higher among the older children suggests that age may play a role in conditioning the site of colonisation. The carriage of respiratory bacteria is strictly age dependent as it is significantly higher in younger children than in adolescents [17], and is modified by vaccine use [18]. Moreover, there are data showing that the primary site of colonisation of bacteria such as Streptococcus pneumoniae can vary with age [19]. As it has been demonstrated that significant interactions can occur between bacterial species and between bacteria and viruses, and that these can affect the carriage rates of a given infectious agent [20], it can be hypothesised that the age-related differences in pharyngeal S. aureus colonisation rates may be due to time-related variations in bacterial balance in different body sites.

Regardless of age, a minority of children showed both oropharyngeal and nasal colonisation. This is different from the findings of some adult studies indicating that bacterial colonisation in the nose is almost always accompanied by colonisation in the throat [7]. However, the difference may be due to the different characteristics of the studied subjects: we only enrolled otherwise healthy children with little or no exposure to the healthcare system, whereas the adult studies mainly involved hospitalised patients. Furthermore, the adult studies also showed that dual colonisation is significantly more frequent in subjects in close contact with other S. aureus carriers, such as frequently hospitalised patients [9].

Although it has not been established what risk oropharyngeal carriers represent in terms of bacterial spread and infection, the findings of this study highlight the importance of adding throat to nasal screening when monitoring the circulation of S. aureus in the community. The additional cost of throat screening could be minimised by pooling samples in the laboratory and, as in this study, using molecular methods that are more cost-effective for screening S. aureus than traditional cultures because of the high cost of unnecessary isolation [21].