Published online August 1, 2006
PEDIATRICS Vol. 118 No. 2 August 2006, pp. 469-474 (doi:10.1542/10.1542/peds.2006-0254)
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ARTICLE

Methicillin-Resistant Staphylococcus aureus Colonization and Its Association With Infection Among Infants Hospitalized in Neonatal Intensive Care Units

Yhu-Chering Huang, MD, PhDa,b, Yi-Hong Chou, MDb,c, Lin-Hui Su, MSb,d, Rey-In Lien, MDb,c and Tzou-Yien Lin, MDa,b

a Divisions of Pediatric Infectious Diseases
c Neonatology, Chang Gung Children’s Hospital, Kweishan, Taoyuan, Taiwan
b School of Medicine, Chang Gung University, Kweishan, Taoyuan, Taiwan
d Department of Clinical Pathology, Chang Gung Memorial Hospital, Kweishan, Taoyuan, Taiwan


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVES. We conducted this study to assess the rate of methicillin-resistant Staphylococcus aureus colonization and its association with infection among infants hospitalized in methicillin-resistant S aureus–endemic NICUs.

METHODS. Between March 2003 and February 2004, surveillance culture specimens from the nares, postauricular areas, axillae, and umbilicus of infants admitted to the NICUs at a children’s hospital in Taiwan were obtained weekly for the detection of methicillin-resistant S aureus. All colonized and clinical isolates from each study infant with methicillin-resistant S aureus infection were genotyped with pulsed-field gel electrophoresis, with Sma1 digestion, and compared.

RESULTS. A total of 783 infants were included in this study. Methicillin-resistant S aureus colonization was detected for 323 infants during their NICU stays, with detection with the first 2 samples for 89%. Nares and umbilicus were the 2 most common sites of initial colonization. Methicillin-resistant S aureus colonization was associated significantly with premature birth (≤28 weeks) and low birth weight (≤1500 g), and infants with colonization had a significantly higher rate of methicillin-resistant S aureus infection, compared with those without colonization (26% vs 2%). Methicillin-resistant S aureus colonization was noted for 84 of 92 infants with methicillin-resistant S aureus infections. Of the 68 episodes with previous colonization and isolates available for genotyping analysis, colonized and clinical isolates were indistinguishable in 63 episodes, highly related in 2 episodes, and distinct in 3 episodes.

CONCLUSIONS. More than 40% of the hospitalized infants were colonized with methicillin-resistant S aureus during their stay in methicillin-resistant S aureus–endemic NICUs; this was associated significantly with methicillin-resistant S aureus infection. Most infants with methicillin-resistant S aureus infections had previous colonization with an indistinguishable strain.

Key Words: methicillin-resistant Staphylococcus aureus • colonization • infection • genotyping analysis • neonatal intensive care unit

Abbreviations: MRSA—methicillin-resistant Staphylococcus aureus • HCW—health care worker • PFGE—pulsed-field gel electrophoresis • MLST—multilocus sequence typing • OR—odds ratio • CI—confidence interval

Methicillin-resistant Staphylococcus aureus (MRSA) is among the most important pathogens of bacteremia in the ICU. Colonized patients are the chief source of S aureus in hospitals. Colonizing strains may serve as endogenous reservoirs for overt clinical infections or may spread to other patients.1–8 One study demonstrated the link between S aureus isolated from blood and S aureus isolated from nasal specimens, taken before and after bacteremia was detected, with the use of molecular methods.9 Most studies were conducted among adults, however, and no study has investigated such a link among infants hospitalized in NICUs.

In Taiwan, 50% to 80% of the S aureus isolates causing nosocomial infections in 12 major hospitals in 2000 were methicillin resistant.10 In our NICUs, MRSA has been among the most common nosocomial pathogens and accounted for >90% of S aureus isolates since 1998.11 Standard infection control measures were implemented but were unable to control the spread of MRSA effectively. To identify infants with MRSA colonization and to implement cohort care for these infants, we screened routinely for MRSA carriage for each infant admitted or transferred to the NICUs. We thus had the opportunity to evaluate the MRSA colonization rate among these infants and its association with the MRSA infection rate, with molecular methods.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Chang Gung Children’s Hospital is a university-affiliated teaching hospital, situated in northern Taiwan, that provides a range of care, from primary to tertiary care, and is a part of Chang Gung Memorial Hospital. There are 3 level III NICUs, distributed on 2 floors, in this children’s hospital. Currently, there are 17, 20, and 12 beds in NICUs 1, 2, and 3, respectively.

Infants admitted to NICUs 1 and 2 in March 2003 to February 2004 were included in this study, and specimens from the nares, postauricular areas, axillae, umbilicus, and perineum were obtained weekly (every Monday) and sent for detection of MRSA. Because of a low yield rate, perineum specimens were discontinued 1 month after commencement of the study. The infants with MRSA colonization were separated from noncolonized infants and placed in a segregated area of the NICUs, and cohort care by designated nurses was implemented.

All infants were observed if they were infected with MRSA. If a study infant with MRSA colonization had MRSA clinical isolates, then the clinical isolates as well as the colonized isolates were genotyped and compared. MRSA isolates recovered from clinical diagnostic samples (beyond surveillance culture specimens) submitted to the clinical microbiology laboratory were regarded as clinical isolates. In accordance with the standard definition of nosocomial infection,12 any infant with clinical isolates of MRSA who was receiving antimicrobial therapy was categorized as experiencing an episode of infection. Episodes of MRSA infection involving a single infant were considered to be distinct if they were ≥2 weeks apart, a course of effective antibiotics had been administered, the clinical symptoms had resolved, and ≥1 negative culture from the infected site was documented.

Three surveillance cultures for health care workers (HCWs) were performed, at the beginning, middle, and end of the study period, and specimens were obtained from the nares of HCWs working in both units. Intranasal mupirocin treatment was administered to each HCW with MRSA colonization.

Surveillance specimens for culture were obtained with a cotton swab, placed in transport medium (Venturi Transystem; Copan Innovation Ltd, Limmerick, Ireland), and then processed in our microbiology laboratory within 4 hours. Identification of MRSA was confirmed according to National Committee for Clinical Laboratory Standards guidelines.13 Pulsed-field gel electrophoresis (PFGE) with SmaI digestion was used in this study to fingerprint the MRSA isolates, according to the procedures described previously.14 The criteria proposed by Tenover et al15 were used for analysis of the DNA fingerprints generated with PFGE. The genotypes were designated, as in our previous studies,14,16–19 in alphabetical order; any new type, if identified, was designated consecutively. PFGE patterns with <4-band differences from an existing genotype were defined as subtypes of that genotype and were labeled with Arabic number suffixes. Two isolates were considered to be indistinguishable, highly related, or distinct if they had the same subtype, the same genotype, or a different type, respectively.

Multilocus sequence typing (MLST) was performed for some selected strains with representative PFGE patterns, as described elsewhere.20 The allelic profiles were assigned through comparison of the sequences at each locus with those of the known alleles in the S aureus MLST database and were defined as sequence types accordingly.

We compared the characteristics of the infants with and without MRSA colonization with {chi}2 tests (continuity-adjusted) or Student’s t tests. Relative risks and/or odds ratios (ORs) were calculated with 95% confidence intervals (CIs). Statistical analyses of the data were performed with EpiInfo, version 6 (Centers for Disease Control and Prevention, Atlanta, GA) and SAS for Windows, version 6.11 (SAS Institute, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the study period, a total of 898 infants were admitted to these NICUs, and 783 infants were included in this study. Of the 783 infants, 13 were transferred to the special care nursery but later were transferred back to the NICUs. A total of 442 infants (56%) were male, 399 infants (51%) were inborn, 468 infants (60%) were premature, and 509 infants (65%) were admitted to the NICUs within 24 hours of life (Table 1). A total of 1925 samples were obtained from the study infants, with a mean of 2.43 samples per infant (range: 1–27 samples).


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  		TABLE 1. Comparison of Demographic Features for Infants Hospitalized in NICUs, With and Without MRSA Colonization

 
Positive results were noted in 1341 specimens from 323 infants (41%), with a mean of 4.15 specimens per colonized infant (range: 1–53 specimens). Of the 323 infants with colonization, 202 infants (63%) had ≥2 sites of colonization. Nares (229 infants, 71%) and umbilicus (195 infants, 60%) were the 2 most common sites of colonization. The sensitivities of nares and umbilicus for the detection of MRSA colonization were 71% and 60%, respectively. The sensitivity could reach 90% if both nares and umbilicus were sampled. Colonization was identified in the first sampling for 222 infants (69%) and in the first 2 samplings for 287 infants (89%). The distributions of the sites of initial colonization are shown in Table 2. Compared with no colonization, MRSA colonization was associated significantly with premature birth (gestational age of ≤28 weeks) and low birth weight (≤1500 g) (Table 1).


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  		TABLE 2. Timing and Site of Initial MRSA Colonization for 326 Infants Hospitalized in NICUs

 
A total of 224 MRSA clinical isolates were identified from 92 infants (12%) during the study period. Colonization was detected for 84 (91%) of the 92 infants, either before (64 infants), concurrent with (6 infants), or after (14 infants) the MRSA infections. Among the 14 infants with later colonization, surveillance cultures for 8 infants had not yet been initiated when the clinical isolates were identified. Among the 64 infants with prior colonization, the interval from the detection of colonization to the MRSA infection ranged from 1 day to 93 days (mean: 13.7 days; median: 10 days). The distribution was as follows: ≤7 days, 26 infants; 8 to 14 days, 17 infants; 15 to 21 days, 9 infants; 22 to 29 days, 8 infants; ≥30 days, 4 infants. The infants with MRSA colonization had a significantly higher rate of MRSA infection than did those without colonization (26% vs 2%; P < .00001; relative risk: 2.64; 95% CI: 2.34–2.98). MRSA infection among these infants was associated significantly with MRSA colonization (P < .00000005; OR: 19.86; 95% CI: 9.11–45.07). MRSA colonization with infection was associated significantly with low birth weight (≤1000 g; P < .0005; OR: 3.79; 95% CI: 1.69–8.51) and premature birth (gestational age of ≤28 weeks; P < .0005; OR: 3.33; 95% CI: 1.66–6.70), compared with colonization but not infection.

A total of 121 clinical isolates from 64 infants with 84 episodes of infection were available for genotyping analysis. Twenty-six infants (41%) had ≥2 clinical isolates available (up to 8 isolates). The source of the 121 clinical isolates included bloodstream (19 isolates), sputum (most from endotracheal tubes aspirates) (64 isolates), central venous catheter (5 isolates), pus (24 isolates), urine (4 isolates), and others (5 isolates). From the 64 infants, 464 colonized isolates were collected and subjected to genotyping analysis together with the 121 clinical isolates. Of the 585 MRSA isolates, 3 genotypes (designated types A, C, and D), with 23 subtypes, were identified (Table 3). The largest population (521 isolates, 89%) belonged to genotype A (similar to Brazilian or Hungary clone), among which the most prevalent subtype, A10, accounted for 316 colonized isolates (68%) and 76 clinical isolates (63%) from 37 infants (58%). The clinical isolates from the same infant were indistinguishable for 23 of the 26 infants with multiple clinical isolates. For the remaining 3 infants, the clinical isolates were highly related, although not indistinguishable. All colonized isolates from the same infant were indistinguishable or highly related for all except 5 infants for whom 1 or a few distinct strains were identified.


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  		TABLE 3. Resolution of PFGE Patterns of 121 Clinical and 464 Colonized MRSA Isolates From 64 Infants Hospitalized in NICUs

 
Of the 64 infants with 84 episodes of MRSA infection, previous colonization was detected for 68 episodes (81%); the clinical isolates and colonization isolates were considered to be indistinguishable in 63 episodes (93%), highly related in 2 episodes, and distinct in 3 episodes, on the basis of PFGE analyses. Of the 16 episodes without previous colonization, surveillance sampling had not yet commenced in 7 episodes. Colonization was detected after clinical isolates were identified in 9 episodes, among which the colonized strains were considered to be indistinguishable from the clinical isolates in 5 episodes, highly related in 1 episode, and distinct in 3 episodes (Table 4).


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  		TABLE 4. Association Between Colonized and Clinical MRSA Isolates From 57 Infants With 77 Episodes of Possible Infections

 
Surveillance cultures for the HCWs working in the 2 NICUs were performed 3 times during the study period, and the nasal MRSA carriage rates were 4.8% (6 of 124 samples), 13% (18 of 138 samples), and 4.9% (6 of 123 samples). Of the 30 isolates recovered, 23 (77%) belonged to genotype C, 5 to genotype A10, and 1 each to genotypes AB and AC (Table 5). One nurse had positive results in all 3 surveillance cultures, and the genotypes of the 3 isolates were C2, C2, and C14.


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  		TABLE 5. Surveillance Cultures for Nasal Carriage of MSRA Among HCWs in NICUs

 
MLST was performed for 9 selected strains with representative PFGE patterns and revealed that 4 strains of PFGE genotype A (A3, A10, A13, and A25) were sequence type 239 (Brazilian or Hungary clone), whereas 3 strains of genotype C (C2, C9, and C17) and 2 strains of genotype D (D13 and D) were all sequence type 59.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Results from this study showed that MRSA clinical isolates were identified for 12% of the hospitalized infants and were associated significantly with MRSA colonization. Previous or concurrent colonization was detected for >80% of the infants with MRSA infection, and the clinical isolates were indistinguishable from the colonized isolates in >90% of the episodes, on the basis of molecular evidence. Like the previous reports for adults,9 an association between MRSA colonization and infection was demonstrated for the neonates. The questions of whether decolonization of these infants could reduce the subsequent infection rate21–24 and which disinfectants are useful deserve additional study.

In this study, MRSA colonization was detected for 41% of the infants admitted or transferred to the NICUs. The rate, although very high, was not beyond prediction, because most infants were premature, with birth weights of ≤1500 g, longer stays in the NICUs were usually required, and they might thus acquire MRSA colonization during their stays in the NICUs. As expected, MRSA colonization in this study was associated significantly with premature birth (gestational age of <28 weeks) and low birth weight (≤1500 g). What was unexpected was that nearly 90% of the colonized infants were detected with the first 2 samples. Because most infants (60%) were admitted to our NICUs within the first 24 hours of life, the acquisition of MRSA by these infants would have occurred very soon after hospitalization or even before the infants were admitted to our NICUs. These findings suggest that the infants might have acquired MRSA from their mothers. However, maternal vaginal colonization of MRSA and its association with results for the neonates were not investigated in this study. A study is being conducted regarding this issue, because community-acquired MRSA infection (28%–74%) and colonization (1.9%–5.3%) among children without risk factors are seen not infrequently in Taiwan.17–19,25–28

Nares are considered to be the most common reservoirs of MRSA and are selected as the sampling sites in most studies regarding MRSA colonization. However, there have been scanty reports in the literature comparing the efficacy of different sampling sites in the neonatal population.29,30 In the current study, although nares and umbilicus were the 2 most common sites of colonization, the sensitivities of nares alone and umbilicus alone for the detection of MRSA colonization were 71% and 60%, respectively. Apparently the sensitivities were insufficient. However, the sensitivity could increase to 90% (negative predictive value: 93%) if both sites were sampled. We think that sampling of these 2 sites is necessary and might be adequate for surveillance cultures in this population.

Our previous study16 indicated that, in 1998 and 2000, genotypes A and C were the 2 major genotypes in these NICUs and accounted for 63% and 35%, respectively, of the MRSA clinical isolates. In the current study, we found that genotype A (sequence type 239, similar to Brazilian or Hungary clone31), particularly a specific subtype (A10), became the only dominant clone and accounted for nearly 90% of all 585 clinical and colonized isolates from the infants. It is intriguing that genotype C accounted for only ~10% of all isolates from the infants, whereas 77% of all isolates from the HCWs belonged to genotype C. These findings suggest that, in addition to the nasal carriage of MRSA by HCWs, there were other factors associated with the spread of MRSA in these units. Cross-transmission among the infants through the transient carriage of MRSA on the hands of HCWs was a strong possibility that requires additional investigation.

From the genotyping results in this study, we also learn that, if an infant hospitalized in a NICU harbors a MRSA strain, then this strain can be found at multiple sites and can exist for a long period (>3 months), resulting in subsequent infection and even recurrent infections. MRSA colonization, acquired either before or after admission, was seen commonly among infants hospitalized in our NICUs, particularly premature infants with very low birth weights. MRSA infection among these infants was associated significantly with previous colonization with an indistinguishable strain.


   ACKNOWLEDGMENTS
 
This study was supported by grants from the National Science Council (NSC 92-2314-B-182A-066) and Chang Gung Memorial Hospital (CMRP 1369).


   FOOTNOTES
 
Accepted Mar 6, 2006.

Address correspondence to Yhu-Chering Huang, MD, PhD, Chang Gung Children’s Hospital, 5 Fu-Shin St, Kweishan, Taoyuan, Taiwan. E-mail: ychuang{at}adm.cgmh.org.tw

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics

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