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Antimicrob Agents Chemother. Mar 2012; 56(3): 1418–1426.
PMCID: PMC3294909

Changing Trends in Antimicrobial Resistance and Serotypes of Streptococcus pneumoniae Isolates in Asian Countries: an Asian Network for Surveillance of Resistant Pathogens (ANSORP) Study

Abstract

Antimicrobial resistance in Streptococcus pneumoniae remains a serious concern worldwide, particularly in Asian countries, despite the introduction of heptavalent pneumococcal conjugate vaccine (PCV7). The Asian Network for Surveillance of Resistant Pathogens (ANSORP) performed a prospective surveillance study of 2,184 S. pneumoniae isolates collected from patients with pneumococcal infections from 60 hospitals in 11 Asian countries from 2008 to 2009. Among nonmeningeal isolates, the prevalence rate of penicillin-nonsusceptible pneumococci (MIC, ≥4 μg/ml) was 4.6% and penicillin resistance (MIC, ≥8 μg/ml) was extremely rare (0.7%). Resistance to erythromycin was very prevalent in the region (72.7%); the highest rates were in China (96.4%), Taiwan (84.9%), and Vietnam (80.7%). Multidrug resistance (MDR) was observed in 59.3% of isolates from Asian countries. Major serotypes were 19F (23.5%), 23F (10.0%), 19A (8.2%), 14 (7.3%), and 6B (7.3%). Overall, 52.5% of isolates showed PCV7 serotypes, ranging from 16.1% in Philippines to 75.1% in Vietnam. Serotypes 19A (8.2%), 3 (6.2%), and 6A (4.2%) were the most prominent non-PCV7 serotypes in the Asian region. Among isolates with serotype 19A, 86.0% and 79.8% showed erythromycin resistance and MDR, respectively. The most remarkable findings about the epidemiology of S. pneumoniae in Asian countries after the introduction of PCV7 were the high prevalence of macrolide resistance and MDR and distinctive increases in serotype 19A.

INTRODUCTION

Streptococcus pneumoniae is one of the most important pathogens causing various types of mucosal and invasive infections with significant mortality worldwide. The disease burden of pneumococcal infections has increased due to widespread emergence of antimicrobial resistance in many countries during the past few decades (17). Previous reports documented very high prevalence rates of beta-lactam and macrolide resistance in S. pneumoniae in Asian countries (6, 7, 11). Particularly, erythromycin resistance has remarkably increased in many Asian countries, where >70% of clinical isolates were fully resistant (17, 23, 24). A previous surveillance study by the Asian Network for Surveillance of Resistant Pathogens (ANSORP) showed that 53.1% of pneumococcal isolates from Asian countries, up to 92% in Vietnam, were resistant to erythromycin (23). In addition, multidrug resistance (MDR) was also very prevalent in Asian countries: 71.4% in Vietnam, 45.9% in South Korea, and 44.9% in Hong Kong (18, 23), rates which were much higher than those in other parts of the world (17, 18, 23).

After the introduction of heptavalent pneumococcal conjugate vaccine (PCV7), the epidemiology of S. pneumoniae has been changing in many countries (1, 8). One of the most prominent changes is the emergence of nonvaccine serotypes such as serotype 19A worldwide (20). According to recent data from the United States in 2007, 93.2% of penicillin-nonsusceptible isolates which caused invasive diseases showed non-PCV7 serotypes, and serotype 19A accounted for 53.2% of these penicillin-nonsusceptible isolates (5). However, since the introduction of PCV7 to Asian countries, the epidemiology of S. pneumoniae in Asian countries has not been well investigated (21, 26). Therefore, the ANSORP Study Group performed a prospective, multinational, hospital-based surveillance study in patients with pneumococcal infections in 11 Asian countries during 2008 to 2009 to investigate the current status of antimicrobial resistance and serotype distribution in S. pneumoniae after the introduction of PCV7.

MATERIALS AND METHODS

Pneumococcal isolates.

S. pneumoniae isolates were prospectively collected from patients with community-acquired pneumococcal infections at 60 hospitals in 11 Asian countries from March 2008 to December 2009. Pneumococcal isolates were collected from clinical specimens representative of normally sterile body sites, such as blood, cerebrospinal fluid (CSF), pleural fluid, ascites, joint fluid, sinus aspirates, and middle ear aspirates. Isolates from lower respiratory tract specimens were also included only if they were cultured from adequate respiratory specimens from patients with clinical and radiographic findings of pneumonia. Pneumococcal isolates from throat swab, nasal swab, or nasopharyngeal aspirate specimens were excluded from this study. Isolates obtained from a patient later than 72 h after admission of the patient to the hospital were not included in this study.

Pneumococcal isolates from participating hospitals, except those in China, were transported to the central laboratory (Samsung Medical Center, Seoul, South Korea) in transport tubes containing Ames transport medium (Copan, Brescia, Italy) and stored at −70°C until use. Isolates from Chinese hospitals were transported to the regional laboratories in Beijing, China (Beijing Union Medical College Hospital and Beijing Children's Hospital), and stored until the test using the same methods performed in the central laboratory in South Korea.

In vitro antimicrobial susceptibility test.

In vitro antimicrobial susceptibility tests of pneumococcal isolates were performed by the broth microdilution method according to guidelines of the Clinical and Laboratory Standards Institute (CLSI) (3) against 14 antimicrobial agents: penicillin, amoxicillin, amoxicillin-clavulanic acid, ceftriaxone, cefuroxime, erythromycin, azithromycin, clarithromycin, levofloxacin, moxifloxacin, gatifloxacin, ciprofloxacin, clindamycin, and co-trimoxazole. Interpretive criteria for susceptibility were those indicated in a CLSI document (4). We used two separate interpretive breakpoints for meningeal and nonmeningeal isolates to define penicillin and ceftriaxone resistance: MICs of ≥0.12 and ≥8 μg/ml for parenteral penicillin and ≥2 and ≥4 μg/ml for ceftriaxone for meningeal and nonmeningeal isolates, respectively. The breakpoint for ciprofloxacin resistance was 4 μg/ml (23). S. pneumoniae ATCC 49619 was used as a control strain. MDR was defined as resistance to more than any three antimicrobial agents of different classes tested in this study.

Detection of erm(B) and mef(A) genes.

Erythromycin-resistant S. pneumoniae isolates were subjected to PCR analysis to detect erm(B) and mef(A) genes as described elsewhere (13, 25).

Serotyping.

Serotypes of S. pneumoniae isolates were determined by the capsular quellung method with commercial antisera (Statens Serum Institut, Copenhagen, Denmark), as recommended by the manufacturer. Serotypes 6c and 6d were confirmed by PCR (9).

Statistical analysis.

Statistical analysis was performed by using SPSS for Windows (version 11.5 software package; SPSS, Chicago, IL). Fisher's exact t test or χ2 test was used to determine the significant differences in resistance and serotype proportion, as appropriate.

RESULTS

Collection of pneumococcal isolates.

A total of 2,184 nonduplicate S. pneumoniae isolates were prospectively collected from patients with pneumococcal infections. Among 2,184 strains, specimen sources and the age of the patient were available in 2,021 cases. Of these, the most prevalent specimen source was sputum (69.5%), followed by blood (13.4%), sinus aspirate (4.8%), pleural fluid (2.4%), middle ear fluid (2.3%), and CSF (2.0%). Among the 2,021 isolates, 781 (38.6%) were isolated from children <5 years of age and 541 (26.8%) from elderly patients (≥65 years old). The mean (±standard deviation) patient age was 34.4 (±31.8) years. A total of 2,100 patients, whose clinical data were available, were included in the analysis of demographic and clinical characteristics of patients with pneumococcal infections (Table 1). Of these patients, 1,344 (64.0%) were male and 756 (36.0%) were female. The most common type of infection was pneumonia (80.0%), and 13.5% of patients with pneumonia had concomitant bacteremia. The most common comorbid condition among patients with pneumococcal diseases was smoking (25.3%). In this study, the prevalence of smoking in patients with pneumococcal diseases was highest in Hong Kong (61.2%) followed by China (41.6%) and Taiwan (32.3%).

Table 1
Demographic and clinical characteristics of patients with pneumococcal infection

Antimicrobial resistance in S. pneumoniae.

According to the revised CLSI breakpoints for parenteral penicillin (resistant [R], ≥8 μg/ml for nonmeningeal isolates and ≥0.12 μg/ml for meningeal isolates), prevalence rates of penicillin resistance were 0.7% and 57.5% in nonmeningeal and meningeal isolates, respectively (Table 2). Compared with previous ANSORP studies in Asian countries in 1996 to 1997 (996 clinical isolates), 1998 to 1999 (1,105 nasopharyngeal isolates), and 2000 to 2001 (685 clinical isolates) (14, 22, 23), current data show a persistently high prevalence of penicillin nonsusceptibility in Asian countries if we apply the previous penicillin susceptibility breakpoints (intermediate [I], 0.12 to 1 μg/ml, and R, ≥ 2 μg/ml) (Table 3). However, according to the revised CLSI breakpoints, the prevalence rate of penicillin-nonsusceptible pneumococci (PNSP) in nonmeningeal isolates was only 4.6% and fully resistant isolates were found only in China (2.2%) and South Korea (0.3%).

Table 2
Susceptibilities to antimicrobial agents of Streptococcus pneumoniae isolates from patients with pneumococcal infections in 11 Asian countriesc
Table 3
Changing trends in penicillin and erythromycin resistance among Streptococcus pneumoniae isolates from patients with pneumococcal infections in Asian countries

Ceftriaxone resistance was 3.7% and 0.1% in nonmeningeal and meningeal isolates, respectively (Table 2). Cefuroxime resistance was 53.9% (from 4.4% in Philippines to 70.0% in Vietnam; MIC90, 8 μg/ml), which was higher than previous data from the ANSORP study in 2000 to 2001 (32.4%) (23). In particular, very high rates of resistance to cefuroxime were found in Vietnam (70.0%), South Korea (68.5%), Sri Lanka (68.4%), and China (62.3%).

Resistance to macrolides in pneumococcal isolates was 72.7%, 69.7%, and 68.9% for erythromycin, azithromycin, and clarithromycin, respectively, and resistance rates were highest in China (96.4%), Taiwan (84.9%), and Vietnam (80.7%) (Table 2). Erythromycin resistance was more frequently found in children (<5 years old; 44.8%) than in adults (≥65 years old; 25.1%) (odds ratio [OR], 2.9; 95% confidence interval [CI], 2.2 to 3.8; P < 0.0001). Compared with the previous data from Asian countries found by ANSORP, erythromycin resistance has markedly increased (P < 0.0001) in Asian countries, particularly in China and Sri Lanka, and was persistently high in Hong Kong, South Korea, Taiwan, and Vietnam (Table 3).

The resistance to fluoroquinolones was 1.7%, 0.4%, 1.5%, and 13.4% for levofloxacin, moxifloxacin, gatifloxacin, and ciprofloxacin, respectively, in the region (Table 2). Isolates from Taiwan (6.5%) and South Korea (4.6%) showed the highest rates of levofloxacin resistance.

The overall rate of MDR in pneumococcal isolates was 59.3% (59.4% and 57.5% in nonmeningeal and meningeal isolates, respectively), with the highest MDR rate being 83.3% in China, followed by Vietnam (75.5%), South Korea (63.9%), Hong Kong (62.2%), and Taiwan (59.7%). The most common pattern of MDR was resistance to cefuroxime, erythromycin, clindamycin, and co-trimoxazole (20.2%), followed by resistance to erythromycin, clindamycin, and co-trimoxazole (7.1%). All strains with MDR were resistant to at least one of the macrolides tested.

Distribution of erm(B) and mef(A) genes.

Of 1,588 erythromycin-resistant isolates, erm(B) and mef(A) genes were identified in 969 isolates excluding 619 isolates from China. Of these isolates, 477 (49.2%) carried only erm(B) (MIC90, 128 μg/ml) and 190 (19.6%) carried only mef(A) (MIC90, 16 μg/ml), whereas 287 (29.6%) contained both erm(B) and mef(A) (Table 4). Of the 287 erythromycin-resistant S. pneumoniae isolates with both erm(B) and mef(A), 70.7% displayed the typical macrolide-lincosamide-streptogramin B (MLSB) phenotype, characterized by high-level resistance to macrolides (MIC, ≥64 μg/ml). The most common serotypes among pneumococcal isolates carrying both the erm(B) and mef(A) genes were 19F (61.3%), 19A (16.4%), and 6A (9.8%), while the majority of isolates of serotype 19A (78.3%), 19F (73.0%), or 6A (54.9%) carried both erm(B) and mef(A).

Table 4
Distribution of macrolide resistance determinants among Streptococcus pneumoniae isolates from patients with pneumococcal infections in Asian countriesa

Serotype distribution.

Of 2,184 isolates of S. pneumoniae, 2,166 isolates were serotyped except 18 isolates from China. Major serotypes of S. pneumoniae in the Asian region were 19F (23.5%), 23F (10.0%), 19A (8.2%), 14 (7.3%), 6B (7.3%), and 3 (6.2%) (Table 5), which together accounted for 62.5% of all isolates. The frequencies of serotypes included in PCV7, PCV10, and PCV13 were 52.5%, 55.9%, and 74.5% in all isolates, respectively, while those in invasive isolates were 46.3%, 58.1%, and 78.6%, respectively. The rates of serotypes covered by PCV7 were relatively high in Vietnam (75.1% of all isolates and 70.8% of invasive isolates) and Sri Lanka (73.7% and 88.9%, respectively), while the rates were very low in Philippines (16.1% and 8.2%, respectively). Major serotypes of invasive pneumococcal isolates were 19F (13.7%) and 14 (12.1%), followed by 19A (8.8%), 3 (8.2%), 6B (7.7%), and 23F (6.9%), accounting for 57.3% of all invasive isolates. The prevalences of serotypes covered by PCV7, PCV10, and PCV13 in S. pneumoniae isolates from children (<5 years old) and adults (≥65 years old) were 62.4% and 46.2%, 63.7% and 47.3%, and 83.8% and 68.8%, respectively. Major serotypes of S. pneumoniae isolated from children (<5 years old) were 19F (33.7%), followed by 19A (13.5%), 14 (10.0%), 23F (9.6%), 6B (7.0%), and 6A (5.8%), which together accounted for 79.5% of isolates. In particular, a high frequency of serotype 19A strains in children (<5 years old) was observed in Taiwan (6/27, 33.3%), China (76/447, 17.0%), and South Korea (10/67, 14.9%). Of the pneumococcal isolates from adults (≥65 years old), 19F (17.0%), 3 (12.4%), 23F (9.8%), 6B (7.9%), 14 (5.5%), and 19A (5.0%) accounted for 57.7% of isolates.

Table 5
Serotype distribution of Streptococcus pneumoniae isolates from patients with pneumococcal infections in 11 Asian countries

Among non-PCV7 serotypes, serotype 3 was more prevalent in adults, particularly in elderly adults aged ≥65 years (54.9%), than in children <5 years old (4.9%), while serotype 19A was more prevalent in children <5 years of age (62.7%) than in adults ≥65 years of age (16.3%).

Compared with the data from a previous ANSORP study in 2000 to 2001 (23), the PCV7 coverage rate has significantly decreased in Asian countries (60.5% in 2000 to 2001 to 52.4% in 2008 to 2009; P = 0.002), while the prevalence of serotype 19A isolates has markedly increased (3% in 2000 to 2001 to 8.2% in 2008 to 2009; P < 0.0001) (Fig. 1).

Fig 1
(A) Serotype distribution of Streptococcus pneumoniae isolates from Asian countries. (B) Distribution of serotype 19A pneumococcal isolates from Asian countries. Data from 2000 to 2001 are from the work of Song et al. (23). Data from Japan in this study ...

Antimicrobial resistance and serotypes.

Among the 1,138 isolates with PCV7 serotypes, 5.5% of isolates (China, 45; Hong Kong, 3; South Korea, 5; Taiwan, 1; Thailand, 2; Vietnam, 7) were PNSP with the revised breakpoints. However, 19.1% of serotype 19A isolates were not susceptible to penicillin, which accounted for 28.1% of PNSP. Among non-PCV7 serotypes, a high prevalence of erythromycin resistance was observed in isolates with serotypes 19A and 6A (86.0% and 85.7%, respectively). Serotype 19A isolates also showed a high prevalence of MDR (79.8%), while non-19A isolates showed a lower prevalence of MDR (58.0%). In particular, a high prevalence of MDR in serotype 19A pneumococci was observed in Hong Kong (100%), China (94.7%), Taiwan (90.9%), and South Korea (90.6%).

DISCUSSION

This study describes the changing trends in antimicrobial resistance and serotype distribution of pneumococcal isolates collected from Asian countries during 2008 to 2009. With regard to the changing trends in antimicrobial resistance in the Asian region, the first remarkable finding was a distinctive and persistent increase in macrolide resistance, which was consistent with other reports (10, 18). Previous ANSORP studies with clinical isolates and nasopharyngeal isolates have already revealed that many Asian countries showed a much higher prevalence of macrolide resistance in pneumococci than did Western countries (14, 22, 23). More seriously, the level of macrolide resistance has remarkably increased with very high MIC90s (64 to ≥128 μg/ml) in China, Hong Kong, Japan, South Korea, Malaysia, Sri Lanka, Taiwan, Thailand, and Vietnam. With regard to the mechanism of macrolide resistance, erm(B)-mediated high-level resistance is the major mechanism in most Asian countries and Europe and is also increasing in the United States recently (10), while the mef(A) gene is still predominant in Canada (16). Compared with our previous study (24), the frequency of macrolide-resistant isolates with erm(B) has increased in Asian countries. An interesting finding was the persistently high prevalence of pneumococci carrying both erm(B) and mef(A) in South Korea (43.3%) and Vietnam (41.0%) and the increased prevalence of those isolates in Hong Kong (8.9% in 1998 to 2001 to 26.4%), Taiwan (0% in 1998 to 2001 to 21.4%), and Thailand (0% in 1998 to 2001 to 11.7%) (24). Major reasons for the high prevalence of macrolide resistance in Asian countries would be widespread use of macrolides in clinical practice and clonal spread of macrolide-resistant strains. Given the current epidemiology of macrolide resistance, an empirical use of macrolides alone for the treatment of community-acquired pneumonia or presumed pneumococcal pneumonia may not be an appropriate choice in many Asian countries, where it may cause the clinical failure of antimicrobial therapy.

The second important finding of pneumococcal resistance in the Asian region was the increasing prevalence of MDR. We found a high prevalence of MDR pneumococci in Asian countries, particularly in China, Vietnam, South Korea, Hong Kong, and Taiwan. The prevalence of MDR pneumococci in Asian countries (59.3%) shown in this study was significantly higher than those reported from other parts of the world such as 9 to 24% in North America and 0 to 43% in Europe (17, 18, 23).

Third, we found a dramatic decrease in the prevalence of penicillin resistance in nonmeningeal isolates according to the revised CLSI breakpoints for resistance to parenteral penicillin, although penicillin MICs have increased in some countries such as China and India compared with our previous studies. Most of the nonmeningeal isolates from Asian countries were susceptible to parenteral penicillin, a finding consistent with other studies worldwide (0 to 7%) (17). However, we found 15 nonmeningeal isolates with a very high level of resistance to penicillin (MIC, ≥8 μg/ml), suggesting that a continued monitoring of PNSP in the region is important.

The overall rates of resistance to fluoroquinolones in pneumococci remained low in most Asian countries, while levofloxacin and gatifloxacin resistance was more frequent in South Korea and Taiwan. We found 10 isolates from South Korea and Taiwan which showed high-level fluoroquinolone resistance with MICs of ≥16 μg/ml for levofloxacin, gatifloxacin, and ciprofloxacin, simultaneously. Therefore, given the popular use of respiratory fluoroquinolones in clinical practice, the emergence of these strains highly resistant to fluoroquinolones could be a concern in the future in the treatment of pneumococcal pneumonia.

With regard to the serotype distribution, this study revealed significant changes in the distribution of serotypes in Asian countries after the introduction of PCV7 vaccination. In the Asian region, the frequency of serotypes covered by PCV7 (52.5%) in this study was lower than 74% and 61% in 1996 to 1997 and 2000 to 2001, respectively (22, 23). PCV7 was recently licensed and introduced into the Asian countries of South Korea (2003); Malaysia, Philippines, and Taiwan (2005); China (2008); and Japan (2009) (19). However, it was included in the National Immunization Program in only a very few Asian countries and areas, including Hong Kong (from 2009), Macau (from 2009), and Singapore (from 2009) (15). Although the PCV7 vaccination rate in most Asian countries has not been investigated, it seems to be very low in most Asian countries due to lack of awareness among both the general public and physicians and due to vaccination cost, while the vaccination rate in children under 5 years of age is relatively high in South Korea (over 60% in urban areas) (12). Vietnam, where PCV7 was not available at the time of the study, showed the highest coverage rate of PCV7 serotypes in this study, while the coverage rates have decreased in most other Asian countries compared with our previous studies. The PCV7 coverage rate in Asian countries was much lower, particularly in Philippines (16.1%), than that in Western countries (80 to 90% in North America and 70 to 75% in Europe) (6). However, the PCV13 coverage rate was 74.5% in overall isolates and 83.8% in isolates from children <5 years of age from Asian countries, which was due to the coverage of non-PCV7 serotypes 19A, 3, and 6A by PCV13.

Emergence of nonvaccine serotypes was associated with increasing prevalence of antimicrobial resistance (8). In the Asian region, serotype 19A was the most prevalent nonvaccine serotype. Compared with our previous ANSORP study in 2000 to 2001 (23), serotype 19A has significantly increased in Asian countries, particularly in China, India, and South Korea. Serotype 19A showed a high rate of penicillin nonsusceptibility, erythromycin resistance, and MDR. The prominent increase in serotype 19A and other non-PCV7 serotypes would be one of the major reasons for a high prevalence of macrolide resistance and MDR in Asian countries. This increase in serotype 19A in Asian countries might be due to the selection of nonvaccine serotypes after PCV7 vaccination, clonal spread of serotype 19A strains (2), or injudicious use of antibiotics in clinical practice.

Since a limited number of isolates were collected from a few hospitals which are mostly located in urban areas, data from this study may not reflect the national status of antimicrobial resistance and serotype distribution. Therefore, nationwide surveillance of pneumococcal resistance and serotypes is strongly warranted.

The current study has provided updated information and changing trends in antimicrobial resistance and serotype distribution of S. pneumoniae in Asian countries. Data showed an extremely high prevalence of macrolide resistance and an increasing prevalence of MDR in many Asian countries. After the introduction of PCV7 vaccination into Asian countries, a distinctive emergence of serotype 19A was observed which was also associated with the increasing prevalence of antimicrobial resistance in S. pneumoniae in the region. Given the high prevalence of resistance and its clinical impact, continuous surveillance of pneumococcal epidemiology and active application of pneumococcal vaccination that can cover non-PCV7 serotypes are strongly warranted in Asian countries.

ACKNOWLEDGMENTS

We thank all investigators of the ANSORP Study Group who have participated in this study for their dedication and contribution. We thank Mi Young Lee and Mihyun Park for their technical support.

This work was partly supported by the Samsung Biomedical Research Institute (SBRI CA72173), Wyeth Pharmaceuticals Inc. (currently, Pfizer Inc.) (0877X1-4448), and the Asia Pacific Foundation for Infectious Diseases (APFID), Seoul, South Korea.

Hospitals and investigators participating in this ANSORP study are as follows: Jae-Hoon Song (Organizer) and Doo Ryeon Chung, Kyong Ran Peck, and Cheol-In Kang (Samsung Medical Center, Seoul); Joon-Sup Yeom (Kangbuk Samsung Hospital, Seoul); Hyun Kyun Ki (Konkuk University Hospital, Seoul); Jun Seong Son (Kyunghee University Hospital, Seoul); Yeon-Sook Kim (Chungnam National University Hospital, Daejeon); Ji-Young Rhee (Dankook University Hospital, Cheonan); Sook-In Jung and Kyung Hwa Park (Chonnam National University Hospital, Gwangju); Shin-Woo Kim and Hyun-Ha Chang (Kyungpook National University Hospital, Daegu); Ki Tae Kwon (Daegu Fatima Hospital, Daegu); Hyuck Lee (Dong-A University Hospital, Busan); Chisook Moon (Inje University Busan Paik Hospital, Busan); Sang Yop Shin (Cheju National University Hospital, Jeju); and Snag Taek Heo (Gyeongsang National University Hospital, Jinju; currently at Cheju National University Hospital, Jeju) in South Korea; Hui Wang (Beijing Union Medical College Hospital, Beijing; currently at Peking University People's Hospital, Beijing); Bin Cao and Yingmei Liu (Beijing Chaoyang Hospital, Beijing); Yunjian Hu and Tieyiing Sun (Beijing Hospital, Beijing); Chao Zhuo and Danhong Su (Guangzhou Institute of Respiratory Diseases, Guangzhou); Yunsong Yu and Yang Qing (First Affiliated Hospital of College of Medicine, Zhejiang University, Hangzhou); Rong Zhang (Second Affiliated Hospital of College of Medicine, Zhejiang University, Hangzhou); Ziyong Sun and Shengdao Xiong (Tongji Hospital of Tongji Medical College, Huazhong University of Sciences and Technology, Wuhan); Yong Liu (Shengjing Hospital of China Medical University, Shenyang); Yunzhou Chu, Baiyi Chen, and Xiaochun Ma (The First Hospital China Medical University, Shenyang); Yonghong Yang, Xuzhuang Shen, Sangjie Yu, Kaihu Yao, and Yinghui Hu (Beijing Children's Hospital Affiliated to Capital Medical University, Beijing); Libo Wang and Chuangqing Wang (Pediatric Hospital of Fudan University, Shanghai); Yuan Chen, Ying Huang, and Lan Liu (Chongquing Children's Hospital, Chongquing); Yuejie Zheng (Shenzhen Children's Hospital, Shenzhen); and Min Lu, Hong Zhang, and Quan Lu (Shanghai Children's Hospital, JiaoTong University) in China; Thomas M. K. So and Tak Keung Ng (Princess Margaret Hospital) and Wai-Keung Kwan and Wing-kin To (Yan Chai Hospital) in Hong Kong; Po-Ren Hsueh (National Taiwan University Hospital, Taipei), Cheng-Hsun Chiu and Lin-Hui Su (Chang-Gung Children's Hospital, Taoyuan), and Yen-Hsu Chen (Chung-Ho Memorial Hospital, Kaohsiung) in Taiwan; Visanu Thamlikitkul (Siriraj Hospital, Bangkok) and Anan Chongthaleong (Chulalongkorn University Hospital, Bangkok) in Thailand; Rohani M. Yasin and Norazah Ahmad (Institute for Medical Research, Kuala Lumpur); Adeeba Kamarulzaman, Sasheela Vanar, and Rina Karunakaran (University Malaya Medical Centre, Kuala Lumpur); Dato' Jeyaindran Sinnadurai, Shanti Rudra Deva, and Mohamad Nazri Aziz (Hospital Kuala Lumpur, Kuala Lumpur); Tan Kah Kee, Suhailah M. Hanapiah, Jaideep Singh Sidhu, and Jenny Tong May Geok (Hospital Seremban, Seremban); Mahiran Mustafa, Nurahan Binti Maning, and Shaiful Azman Zakaria (Hospital Kota Bharu, Kelantan); Christopher Lee, Anuradha, Radhakrishnan, Shanti Ratnam, Zubaidah Abdul Wahab, and Ariza Adnan (Hospital Sungai Buloh, Sungai Buloh, Selangor); Lily Ng, Timothy William, Kausalia Chinnaiah, and Azura Hussin (Hospital Queen Elizabeth, Pulau Pinang); Ganeswrie Balan, Subramaniam Balan, Chua Hoch Hin, Tan Cheng Cheng, and Kan Foong Kee (Hospital Sultanah Aminah, Johor Bahru); Salbiah Hj Nawi, Loh Eng Chang, and Tang Swee Ping (Hospital Salayang, Kuala Lumpur); and Ahmad Kashfi Abd Rahman, Siow Yen Ching, Mohd Ridwan Mohd, Noor, Jimmy Lee Kok Foo, Fatimah Haslina Abdullah, and Noraznita Safie (Hospital Tuanku Nur Zahira, Kuala Terengganu) in Malaysia; Celia Carlos (Research Institute for Tropical Medicine, Manila), Sullian Naval (The Lung Center of the Philippines, Quezon), Media Dora Saniel (The Medical City, Pasig), Joanne Lobo (Davao Medical Center, Davao), Consuelo Malaga (Vicente Sotto Memorial Hospital), and Thea Pamela Cajulao and Xenia Fabay (Baguio General Hospital and Medical Center, Baguio City) in Philippines; Pham Hung Van and Pham Thai Binh (University of Medicine and Pharmacy, Ho Chi Minh City), Tran Van Ngoc and Tran Thi Thanh Nga (Cho Ray Hospital, Ho Chi Minh City), Le Tien Dung (Nguyen Tri Phuong Hospital, Ho Chi Minh City), Doan Mai Phuong (Bach Mai Hospital, Ha Noi), Tung Vu Nguyen (National Institute of Tropical Diseases, Ha Noi), Huyen Dieu Thi Phan (Hospital C in Da Nang, Da Nang), and Chau Vinh (Tropical Diseases Hospital, Ho Chi Minh City) in Vietnam; M. K. Lalitha (Chennai Medical Mission, Chennai), Saradha Suresh (Institute of Child Health, Chennai), and Ranganathan Iyer (Global Hospital, Hyderabad) in India; Nobuyuki Shimono and Yujiro Uchida (Kyushu University Hospital, Fukuoka) in Japan; Jennifer Perera (University of Colombo, Colombo) in Sri Lanka; and Atef M. Shibl (King Saud University Hospital, Riyadh) in Saudi Arabia.

Footnotes

Published ahead of print 9 January 2012

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