Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Taiwanese Children in 2005 and 2006.

J

OURNAL OF

C

LINICAL

M

ICROBIOLOGY

, Dec. 2007, p. 3992–3995

Vol. 45, No. 12

0095-1137/07/$08.00

⫹0 doi:10.1128/JCM.01202-07

Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal

Colonization among Taiwanese Children in 2005 and 2006

䌤

Yhu-Chering Huang,

1,3

* Kao-Pin Hwang,

2,3

Po-Yen Chen,

4

Chih-Jung Chen,

1,3

and Tzou-Yien Lin

1,3

Division of Pediatric Infectious Diseases, Chang Gung Children’s Hospital and Chang Gung Memorial Hospital at Linko

1

_and

Kaohsiung,

2

_{Taiwan; College of Medicine, Chang Gung University, Taoyuan, Taiwan}

3

_{; and Department of Pediatrics,}

Taichung Veterans General Hospital, Taichung, Taiwan

4

Received 15 June 2007/Returned for modification 20 August 2007/Accepted 4 October 2007

From July 2005 to October 2006, a total of 3,046 children, of ages between 2 months and 5 years,

presented for a well-child health care visit to one of three medical centers, which are located in the

northern, central, and southern parts of Taiwan, and were surveyed for nasal carriage of

methicillin-resistant Staphylococcus aureus (MRSA). The overall prevalences of S. aureus and MRSA nasal carriage

among the children were 23% and 7.3%, respectively (18% and 4.8% in the central region, 25% and 6.7%

in the southern region, and 27% and 9.5% in the northern region). Of the 212 MRSA isolates (96%)

available for analysis, a total of 10 pulsed-field gel electrophoresis (PFGE) patterns with two major

patterns (C [61%] and D [28%]) were identified. One hundred forty-nine isolates (70%) contained type IV

staphylococcal cassette chromosome mec (SCCmec) DNA, and 55 isolates (26%) contained SCCmec V

T

.

The presence of Panton-Valentine Leukocidin (PVL) genes was detected in 60 isolates (28%). Most MRSA

isolates belonged to one of two major clones, characterized as sequence type 59 (ST59)/PFGE C/SCCmec

IV/absence of PVL genes (59%) and ST59/PFGE D/SCCmec V

T

/presence of PVL genes (25%). We concluded

that between 2005 and 2006, 7.3% of healthy Taiwanese children were colonized by MRSA in nares. MRSA

harbored in healthy children indicates an accelerated spread in the community.

Recent reports indicate that community-acquired

methicil-lin-resistant Staphylococcus aureus (CA-MRSA) infections are

increasing worldwide and may now involve persons without

risk factors predisposing them for acquisition (2, 11–14, 20,

24). Asymptomatic CA-MRSA colonization has been

docu-mented in healthy children attending the emergency

depart-ments and outpatient clinics of children’s hospitals (6, 19, 25,

27, 28).

Carriage of S. aureus, including MRSA, is well known to be

a significant risk factor for subsequent infection (7, 29), and the

anterior nares are the most consistent sites of colonization.

The presence of S. aureus nasal colonization can provide an

indication of a high risk for subsequent infection.

In Taiwan, previous reports (1, 3, 9, 15, 17, 23, 31) have

indicated that during the period from 1997 to 2003, MRSA

accounted for 9.8% to 36% of CA S. aureus infections in

children without risk factors and the MRSA colonization rate

in the general population ranged from 1.9% to

⬃3.3% for

school children and 5.3% for healthy children presented for

health care visits to 10.8% for health care workers and 13.6%

for contacts of CA-MRSA infection. It is noteworthy, however,

that most of these studies were conducted in the northern part

of Taiwan and no island-wide survey has yet been conducted to

elucidate this issue. To estimate the extent of MRSA in the

community in Taiwan and to assess if there is an increasing

trend of MRSA nasal colonization in healthy children during

the past 5 years, we conducted this island-wide survey between

2005 and 2006. All collected MRSA isolates were also further

characterized by molecular methods.

MATERIALS AND METHODS

This study was approved by the Institutional Review Board of the Chang Gung Memorial Hospital. From July 2005 to October 2006, all children of ages be-tween 2 months and 5 years who presented for a well-child health care visit to any one of three medical centers in Taiwan were invited to participate in this study. The three medical centers involved were the Chang Gung Children’s Hospitals at Linko (hospital A) and Kaohsiung (hospital C) and Taichung Veterans Gen-eral Hospital (hospital B), which are situated, respectively, in northern, southern, and central parts of Taiwan. In each hospital, around 80 subjects were recruited for study for each month, and the ages of the subjects were evenly distributed in seven separate age ranges, which included⬎2 to 6 months, ⬎6 to 12 months, ⬎12 to 18 months, ⬎18 to 24 months, ⬎2 to 3 years, ⬎3 to 4 years, and ⬎4 to 5 years. A culture from the anterior nares for the detection of MRSA was obtained from each subject after written consent was obtained from their par-ents/guardians.

Survey specimens for culture were obtained with a cotton swab, placed in the transport medium (Venturi Transystem; Copan Innovation Ltd., Limerick, Ire-land), and then brought to and processed in the microbiological laboratories within 4 hours of the sampling. All S. aureus isolates were sent to Chang Gung Memorial Hospital at Linko for microbiological characterization. Identification of MRSA was confirmed according to Clinical and Laboratory Standards Insti-tute 2005 guidelines (5). Pulsed-field gel electrophoresis (PFGE) with SmaI digestion was used in this study to fingerprint the MRSA isolates and was performed according to procedures described previously (3, 16, 18). The geno-types were designated in alphabetical order, as in our previous studies (3, 15–18); any new genotype, if identified, was designated consecutively. PFGE patterns with fewer than four band differences from an existing genotype were defined as subtypes of that genotype.

SCCmec typing of isolates was done using a multiplex PCR strategy described previously (26). Control strains for SCCmec types I, II, III, and IVa, kindly provided by Keiichi Hiramatsu, were as follows: type I, NCTC10442; type II, N315; type III, 85/2082; and type IVa, JCSC4744. SCCmec typing for type VTwas determined by using a particular primer described elsewhere (1), and strain TSGH-17, kindly provided by Chi-Chien Wang, was used as a control. However, the SCCmec typing method for type VTyielded inconsistent results; thus, an

* Corresponding author. Mailing address: Chang Gung Children’s

Hospital, Department of Pediatrics, 5, Fu-Shin Street, Kweishan,

Taoyuan, Taiwan. Phone: 3281200, ext. 8202. Fax:

886-3-3288957. E-mail: ychuang@adm.cgmh.org.tw.

䌤

_{Published ahead of print on 17 October 2007.}

alternative method was used. The appearance of an isolate with only two bands (414 bp and 243 bp) in the multiplex PCR analysis may have indicated that the isolate contained SCCmec VT. To confirm their identities, a novel pair of prim-ers, ccrC-5F (5⬘-CAC TTA ATC CAT TGA CAC AG-3⬘) and ccrC-5R (5⬘-AAA GAT TGA GGG ATA AGA CT-3⬘), was designed according to the published sequence (GenBank accession no. AY894416) of the ccrC gene of a Taiwanese strain, S. aureus TSGH-17. Amplification of a specific 1,081-bp DNA fragment, which was subjected to further sequence analysis for some representative isolates in preliminary experiments, confirmed that the isolates contained SCCmec VT. The presence of Panton-Valentine leukocidin (PVL) genes was determined by a PCR strategy described previously (22). Some isolates of representative PFGE patterns were selected and underwent multilocus sequence typing (MLST) as described elsewhere (8). 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.

RESULTS

During the study period, 1,279 subjects were recruited from

hospital A, 1,011 subjects from hospital B (from July 2005 to

June 2006), and 756 subjects from hospital C (from October

2005 to June 2006). All the children enrolled are Taiwanese.

The number of subjects enrolled in each age group ranged

from 430 for children of ages

⬎6 to 12 months to 443 for

children of ages

⬎2 to 3 years. Of the total of 3,046 subjects

enrolled in this study, 713 (23%) were colonized with S. aureus.

Of the 713 isolates, 221 (31%) were demonstrated to be

MRSA. The details of the nasal MRSA colonization

preva-lence for subjects in the different parts of Taiwan are shown in

Table 1. The MRSA colonization rate in northern Taiwan was

significantly higher than that in the central (P

⬍ 0.001) and

southern (P

⬍ 0.039) parts of Taiwan. The nasal MRSA

col-onization prevalences for the subjects in each age group were

8.4% for the children of ages

⬎2 to 6 months and 6.3%, 3.2%,

3.9%, 9.0%, 9.5%, and 10.1% for children of ages

⬎6 to 12

months,

⬎12 to 18 months, ⬎18 to 24 months, ⬎2 to 3 years,

⬎3 to 4 years, and ⬎4 to 5 years, respectively. For those less

than 18 months of age, the carriage rate decreased with

in-creasing age (P

⫽ 0.0011; Mantel-Haenszel test for trend),

while for those older than 12 months of age, the carriage rate

increased with increasing age (P

⬍ 0.0001).

Of the 221 MRSA isolates, 212 isolates were available for

analysis. All of these 212 isolates were sensitive to vancomycin

and teicoplanin. All but two of the isolates identified from

hospital A were resistant to penicillin. Most isolates were

re-sistant to erythromycin and clindamycin but sensitive to

tri-methoprim-sulfamethoxazole (SXT) and doxycycline. The

de-tailed susceptibility distribution of various antibiotics for the

isolates is shown in Table 2. No significant difference in

anti-biotic susceptibility patterns was noted among the isolates

from the three different regions of Taiwan.

Table 3 illustrates the detailed distribution of PFGE

pat-terns, SCCmec types, and the presence/absence of PVL genes

among these isolates. A total of 10 PFGE patterns were

iden-tified. Patterns C and D were the two most common patterns

and accounted for 62% and 28% of the isolates analyzed,

respectively. The distribution of PFGE patterns among the

three regions showed a trend for a difference (P

⫽ 0.09 by a

log-likelihood contingency test). Four types (types II, III, IV,

and V

T

) of SCCmec genes were identified among the isolates,

with type IV (70%) being the predominant type, followed by

type V

T

(26%). The distribution of SCCmec types among the

three regions was significantly different (P

⫽ 0.03). Four

iso-lates of the AF PFGE pattern were untypeable by the methods

used in this study. PVL genes were present in 60 isolates

(28%). Twenty-five isolates underwent MLST, and eight

se-quence types were identified. Sese-quence type 59 (ST59) was the

most common sequence type and accounted for 9 of 10 PFGE

type C isolates, 4 of 6 PFGE type D isolates, and the isolate of

PFGE type AN. The other two isolates of PFGE type D were

ST338, which is a single-locus variant of ST59 (a single

nucle-otide difference in the gmk locus). The remaining isolate of

PFGE type C belonged to a new sequence type, which is a

single-locus variant of ST59 (a single nucleotide difference in

the pta locus). One isolate of PFGE type F also belonged to a

new sequence type, which is also a single-locus variant of ST9

(a single nucleotide difference in the gmk locus). The detailed

association of PFGE patterns with sequence types and SCCmec

types and the presence of the PVL gene of these isolates are

shown in Table 4. The MRSA isolates characterized by ST59/

PFGE type C/SCCmec IV/absence of PVL genes and ST59/

PFGE type D/SCCmec V

T

/presence of PVL genes were the

two most common clones and accounted for 59% and 25% of

the isolates analyzed, respectively.

TABLE 1. Nasal carriage of MRSA among infants and children

presented for a well-child health care visit in Taiwan

Area of Taiwan No. of subjects No. (%) with S. aureusa No. (%) with MRSAb

Northern

1,279

344 (26.9)

121 (9.5)

Central

1,011

180 (17.8)

49 (4.8)

Southern

756

189 (25)

51 (6.7)

Total

3,046

713 (23.4)

221 (7.3)

a_{The rate of carriage of S. aureus among children in the central region was}

significantly lower than those among children in the northern and southern regions (P⬍ 0.001).

b_{The rate of carriage of MRSA among children in the northern region was}

significantly higher than those among children in the central (P⬍ 0.001) and southern (P⫽ 0.039) regions.

TABLE 2. Antibiotic susceptibility rates of 212 colonizing MRSA isolates from children in Taiwan

Area of Taiwan (na₎

No. (%) of isolates susceptible to:

Penicillin Erythromycin Clindamycin Doxycycline SXT Vancomycin Teicoplanin

Northern (120)

2 (1.7)

10 (8.3)

13 (11)

118 (98)

119 (99)

120 (100)

120 (100)

Central (42)

0

1 (2.4)

3 (7.1)

39 (93)

39 (93)

42 (100)

42 (100)

Southern (50)

0

3 (6)

3 (6)

50 (100)

49 (98)

50 (100)

50 (100)

Total (212)

2 (0.9)

14 (6.6)

19 (9.0)

207 (98)

207 (98)

212 (100)

212 (100)

a_{n, no. of isolates.}

DISCUSSION

Results from this study indicate that the national prevalence

of nasal MRSA colonization among otherwise healthy children

in Taiwan was 7.3% during the period from July 2005 to

Oc-tober 2006 inclusively, with values ranging from 4.8% in the

central region of Taiwan to 9.5% in the northern region of

Taiwan. Compared with those among the healthy children

dur-ing the period of 2001 to 2002 (1, 17, 23) (Table 5), though the

study population was different for these studies, the nasal

MRSA colonization prevalence among healthy children in

Tai-wan increased significantly, from 1.9% in 2001 to 9.5% (P

⬍

0.0001 by chi-square test) during the period of 2005 to 2006 for

northern Taiwan and significantly from 3.3% to 6.7% for

southern Taiwan (P

⬍ 0.001 by chi-square test). This

increas-ing trend of nasal MRSA colonization prevalence might

ac-count for the increasing incidence of CA-MRSA infection in

children in Taiwan (3, 9, 31). In the United States, where

CA-MRSA is also being increasingly reported, the MRSA

col-onization prevalence for the general population appeared to

have been relatively low until the year 2002 (19, 21, 25, 27, 28).

In a survey (21) involving 9,622 persons conducted between

2001 and 2002, national S. aureus and MRSA nasal

coloniza-tion prevalence estimates were 32.4% and 0.8%, respectively.

For healthy children, the nasal colonization rates ranged from

0.2% to 2.2% (19, 25, 27, 28), as reported in several pediatric

studies; however, an increasing trend in this regard has been

noted in certain areas of the United States recently (6). Creech

et al. (6) reported that the nasal MRSA colonization rate

among healthy children in Nashville, TN, increased

signifi-cantly from 0.8% in 2001 to 9.2% in 2004, a picture not

dis-similar to what we show in the present study from Taiwan.

In the United States, CA-MRSA strains have been

recog-nized as representing a novel pathogen which was genetically

different from the nosocomial MRSA strains (14, 24). They

have limited antibiotic resistance (except to

␤-lactams), have

two common PFGE patterns (USA 300 and USA 400), possess

different exotoxin gene profiles (e.g., PVL), and contain SCCmec

DNA (10). In contrast, the CA-MRSA clinical isolates in

Tai-wan were multiresistant and shared two common PFGE

pat-terns (patpat-terns D and C in this study) (1, 3, 4, 30). In the

current study, more than 90% of the MRSA colonization

iso-lates were multiresistant to erythromycin and clindamycin but

sensitive to SXT and doxycycline. In addition, most

coloniza-tion isolates shared common molecular characteristics, and

more than 80% of the isolates belonged to one of two major

clones, characterized by ST59/PFGE type C/SCCmec

IV/ab-sence of PVL genes or ST59/PFGE type D/SCCmec V

T

/pres-ence of PVL genes. However, among the clinical isolates, the

clone characterized by ST59/PFGE type D/SCCmec V

T

/pres-ence of PVL genes was the dominant clone (1, 3, 30), while

among the colonized isolates, the clone characterized by ST59/

PFGE type C/SCCmec IV/absence of PVL genes was

domi-nant. It seemed that PVL genes, reported to be a virulence

factor associated with necrotizing pneumonia and abscesses

(22), may be associated with the ability of a PVL-positive clone

to cause infection.

There existed several limitations in the current study. First,

the demographic characteristics and the risk factors associated

with MRSA acquisition were not analyzed and compared

be-tween the children with and without CA-MRSA colonization,

though all the children were healthy and presented for health

care visits. Living with a family member who works in a

hos-pital or clinic and demographic characteristics (e.g., age and

gender) were reported to be associated with an increased risk

of MRSA colonization (6, 21, 25). Second, the persistence of

MRSA carriage in the subjects could not be determined and

the incidence of subsequent MRSA infection in the subjects

could not be measured in this cross-sectional analysis of

MRSA nasal colonization prevalence.

In summary, 7.3% of healthy children in Taiwan were

colo-nized by MRSA in the nares during the period from 2005 to

2006. MRSA carriage in the children may accelerate the

spread in the community. Two major CA-MRSA clones were

TABLE 3. Distribution of PFGE patterns, SCCmec types, and presence of PVL genes among 212 colonizing MRSA isolates

Area of Taiwan (na₎

No. (%) of isolates with characteristic

PFGE pattern SCCmec typeb

Presence of PVL genes Absence of PVL genes A C D Other II III IV VT

Northern (120)

1 (0.8)

66 (55)

40 (33)

13 (11)

0

0

81 (68)

37 (31)

40 (33)

80 (67)

Central (42)

2 (4.8)

28 (67)

10 (24)

2 (4.8)

0

2 (4.8)

32 (76)

8 (19)

11 (26)

31 (74)

Southern (50)

0

37 (74)

9 (18)

4 (8)

2 (4)

0

36 (72)

10 (20)

9 (18)

41 (82)

Total (212)

3 (1.4)

131 (62)

59 (28)

19 (9.0)

2 (0.9)

2 (0.9)

149 (70)

55 (26)

60 (28)

152 (72)

a_{n, no. of isolates.}

b_{Four isolates were untypeable. The distributions of SCCmec types were significantly different among the three regions (P⫽ 0.03).}

TABLE 4. Association of PFGE patterns with MLST, SCCmec

types, and presence of PVL genes for 212 MRSA isolates

PFGE pattern (na₎ No. of subtypes SCCmec type (n) Status of PVL

genes (n) Sequence type

b

A (3)

3

III (2), IV (1)

Absent

ST239

C (131)

25

IV (129), V

T

(2)

Absent (129),

present (2)

ST59, new*

D (59)

13

V

T

(53), IV

(6)

Present (57),

absent (2)

ST59, ST338*

F (3)

2

II (2), V

T

(1)

Absent

ST5, new*

AF (4)

1

Untypeable

Absent

ST89

AK (2)

2

IV

Absent

ST508

AN (3)

2

IV

Absent

ST59

AQ (5)

3

IV

Absent

ST508

AR (1)

1

IV

Absent

ST15

BA (1)

1

IV

Absent

ST5

a_{n, no. of isolates.}

b_{Each of the three sequence types marked with an asterisk is a single-locus}

variant of ST59, but they differ from each other.

identified and would appear to have spread island-wide.

Fur-ther studies are needed to determine the host factors of

colo-nization and to develop strategies to disrupt transmission of

CA-MRSA to susceptible hosts.

ACKNOWLEDGMENTS

This study was supported by a grant from National Science

Coun-seling of Executive Yuan of Taiwan (NSC95-2314-B182A-145).

We have no financial relationships relevant to this article to disclose.

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TABLE 5. Reported prevalence rates of MRSA nasal colonization for healthy Taiwanese children between 2001 and 2006

Period Area of

Taiwan Subjects Age of subjects

No. of subjects

No. (%) with

MRSAb Reference

2001

Southern

Schoolchildren

2 yr to

⬃18 yr

987

33 (3.3)

Lu et al. (23)

2001-2002

Northern

Schoolchildren

3 yr to

⬃12 yr

262

5 (1.9)

Huang et al. (17)

2003

Northern

Schoolchildren, health care visits

⬍12 yr

640

48 (7.5)

a

_{Boyle-Vavra et al. (1)}

2005-2006

Northern

Children for health care visits

2 mo to

⬃5 yr

1,279

121 (9.5)

This study

Central

Children for health care visits

2 mo to

⬃5 yr

1,011

49 (4.8)

This study

Southern

Children for health care visits

2 mo to

⬃5 yr

756

51 (6.7)

This study

a_{If restricted to those without risk factors, no. of colonized subjects would be 34 (5.3%).}

b_{The prevalence increased significantly in the northern (P⬍ 0.0001 by chi-square test) and southern (P ⬍ 0.001) regions of Taiwan during the period of 2001 to}

2006.