To the best of our knowledge, this is the first comprehensive survey of S. aureus
nasal carriage conducted in Brazil, and it included 1,192 children attending 62 out of a total of 70 public DCCs in Goiânia. The prevalence of S. aureus
nasal colonization in this population (31.1%) was higher than previously detected in S. aureus
carrier children at the moment of hospital admission (13.5%) in the same municipality (21
). Our findings are consistent with those of studies conducted in other DCCs, especially in Asia (15
), and they corroborate the fact that DCCs are a favorable environment for S. aureus
We found that children older than 23 months, those who previously attended other DCCs, and those whose mother had a lower level of education were at higher risk to be colonized by S. aureus
. A possible explanation for the increase in S. aureus
colonization with age may be due to pneumococcal competition at an early age of life, leading to a negative correlation for the cocolonization of S. aureus
and Streptococcus pneumoniae
, as observed by others (2
). In fact, in a previous study among day care attendees in Goiânia, we have shown that children under 24 months of age were preferentially colonized by S. pneumoniae
in contrast to older children, who were colonized by S. aureus
A mother's high level of education was found to be an independent protective factor for S. aureus nasal colonization. This association could not be explained by the number of siblings because no interaction was observed between this variable and the mother's schooling. Education level is a proxy of socioeconomic status, and a low level of maternal education may interfere with the mother's compliance with control measures (such as hand washing) that minimize the spread of S. aureus and MRSA.
It is well recognized that DCCs are efficient settings for the acquisition and transmission of pathogens due to crowded conditions, frequent close physical contact, breakdown in appropriate hygiene, and intensive exposure to antimicrobials. In addition, children with longer time periods of child care exposure are more prone to be colonized by MRSA than children who are attending DCCs for the first time (15
). One intriguing point of this survey is the low prevalence of MRSA in an environment that otherwise would be considered very conducive to spread. Therefore, one may question why the MRSA strains that have entered this population did not spread widely in this DCC environment. Among the 14 MRSA strains found, 8 belonged to clone ST239-III, which is an international epidemic nosocomial clone that is widely spread in hospitals in many countries all over the world. ST239-III is not common in the community unless people attend a health care facility recurrently, which was not the case in our sample of healthy children attending a DCC. Most of the children enrolled in the present study have attended an outpatient service, which explains the acquisition of nosocomial MRSA clones. Even though HA-MRSA clones have been frequently found in the community and though DCCs are considered to be very conducive to the spread of many bacterial pathogens due to close contact, sharing of secretions, heavy antibiotic use, etc., HA-MRSA does not seem to be able to spread in this environment. This is consistent with the fact that CA-MRSA clones are phenotypically and genotypically different from HA-MRSA.
The prevalence of MRSA nasal colonization in this population was estimated to be 1.2%. This rate is within the reported range (0.2 to 13%) of MRSA carriers among healthy children (17
). The majority of MRSA strains were identified as belonging to the most common MRSA clone in Brazil (ST239-III), which is endemic in health care settings all over the country (38
). This cluster is epidemiologically related because half of the isolates were obtained from children attending the same DCC, supporting cross-transmission. In this way, our findings suggest that day care children are acquiring and spreading SCCmec
type III MRSA clones associated with the health care environment into the pediatric community as colonizing pathogens. In fact, studies have indicated that SCCmec
type III is escaping the hospital environment and is adapting to the community (4
In the present study we found a new association, ST12-MRSA-IIIA; ST12 has been previously found in association with SCCmec
type IV only (19
). So far, few reports have detected the presence of ST12 strains. Strains representing ST12 have been described as an uncommon MRSA genetic background, and studies have suggested that these strains come from a sporadic and diverse lineage (3
). Whether these ST12 strains are in a transitional state is an open issue.
Three MRSA strains belonged to ST121. As far as we know, no other ST121-IV isolates from Brazil have been reported. This clone has been found in both health care- and community-associated methicillin-susceptible S. aureus
(MSSA) and in some cases carrying the PVL gene (12
). The emergence of ST121-IV may be the result of a local SCCmec
acquisition by an ST121 MSSA strain (30
). Moreover, ST121 isolates that are also PVL positive have been reported all over the world mainly as MSSA. The chronological order of acquisition of the SCCmec
and PVL genes by the same S. aureus
strain is currently still unclear. It may be that in the present ST121-IV strain, it is a question of fitness cost, with the SCCmec
acquisition occurring preferentially in a background without PVL. A few cases of infection caused by CA-MRSA ST30-IV have been reported in Brazil (32
). These strains were PVL positive, but they were responsible for infection instead of colonization. Because our study addressed only colonization, this may explain (at least partially) the absence of this toxin's genes.
A novel finding of this investigation was the detection of the SCCmec
type V in Brazil, which was assigned to ST1120, a single-locus variant of ST45 differing at the aroE
locus. This is the first report of a Brazilian isolate of SCCmec
V. The strain showed a PFGE profile very similar to the first SCCmec
type V isolate (ST45) recovered in Portugal (1
) and was grouped into clonal complex 45, previously associated with both health care and community environments (16
). Both the Brazilian and Portuguese SCCmec
type V isolates were PVL negative. Although this SCCmec
type V strain was recovered from a healthy child who had been exposed to known risk factors for HA-MRSA (hospitalization and antimicrobial use), its SCCmec
type was compatible with CA-MRSA. Thus, it is not possible to establish the epidemiology of this MRSA strain acquisition. Our findings emphasize the need for continued molecular surveillance of MRSA, with special concern for the dissemination of CA-MRSA into the Brazilian hospital setting.
Limitations of this work should be mentioned. We failed to detect a positive association between carriage of MRSA and variables currently acknowledged as risk factors. A possible explanation could be the small number of MRSA strains isolated in this study, which thus lacks sufficient statistical power for detecting such an expected association. Moreover, the collection of nasal swabs from a single nare may have diminished the detection of MRSA strains.
In our study, no significant association was found between antibiotic usage in the past 6 months and MRSA carriage although more than 80% of the participants had taken antibiotics in the previous 6 months. This indicates that this population is itself a high-risk one, as the participants have attended an outpatient service, which explains the acquisition of nosocomial MRSA clones. Also, the questionnaire did not evaluate the presence of a health care worker in the household as a potential risk factor for both S. aureus and MRSA carriage. However, proxy variables were assessed, such as having any household member admitted to the hospital and family morbidity in the past 6 months, and these could indicate a connection between a household member and the health care environment. Another point to be considered is the fact that this investigation occurred 4 years ago, and the epidemiology of MRSA may have changed significantly since then.
In conclusion, this survey showed that the prevalence of MRSA in a large sample of healthy Brazilian children is still low. However, the horizontal spread of HA-MRSA clones, such as the Brazilian strain of MRSA, may be expected within the pediatric community due to the two-way flow of MRSA dissemination. Moreover, the detection of three isolates belonging to ST121, a clone frequently associated with PVL genes, is of special concern in a young population. Thus, continued monitoring of S. aureus and MRSA in our municipality is advisable in order to establish appropriate educational and infection control measures to disrupt transmission to susceptible hosts.