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Journal of Clinical Microbiology, March 2009, p. 715-720, Vol. 47, No. 3
0095-1137/09/$08.00+0     doi:10.1128/JCM.00747-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Genetic Analysis of Group A Streptococcus Isolates Recovered during Acute Glomerulonephritis Outbreaks in Guizhou Province of China

Ming-huan Zheng,¹ Zhen-quan Jiao,² Li-jie Zhang,³ Sang-jie Yu,⁴ Guang-peng Tang,⁵ Xiao-mei Yan,¹ Li-hua He,¹ Fan-liang Meng,¹ Fei Zhao,¹ Mao-jun Zhang,¹ Di Xiao,¹ Yong-hong Yang,⁴ Wei Nie,⁵ Jian-zhong Zhang,^1* and Zi-jun Wang^2*

Department of Diagnosis, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, People's Republic of China,¹ Office of Disease Control and Emergency Response, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China,² CFETP, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China,³ Beijing Children's Hospital Affiliated to Capital Medical University, Beijing, People's Republic of China,⁴ Center for Disease Control and Prevention of Guizhou Province, Guiyang, People's Republic of China⁵

Received 19 April 2008/ Returned for modification 18 August 2008/ Accepted 22 December 2008

Top ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
In this study, 68 group A streptococcus (GAS) isolates associated with two outbreaks of acute glomerulonephritis (AGN) in China were analyzed by emm typing. A total of 11 different emm types were identified. Analysis of emm type distribution suggested that AGN outbreaks in two counties were caused by emm60.1- and emm63.0-type GAS. These two types were further characterized by pulsed-field gel electrophoresis, multilocus sequence typing, sof sequence typing, and PCR-based identification of streptococcal pyrogenic exotoxin A, B, and C (speA, speB, and speC) genes. In antimicrobial susceptibility tests, all outbreak strains were resistant to erythromycin and tetracycline, and the rates of resistance of nonoutbreak strains to the two antibiotics were 63.6% and 90.9%. This study is also the first to report a nephritogenic M63 GAS strain.

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Acute glomerulonephritis (AGN) is an acute nephritic syndrome characterized by the sudden appearance of edema, hematuria, proteinuria, and hypertension. AGN most often follows a streptococcal infection of the throat or skin. It is recognized that only specific M protein serotypes of group A streptococcus (GAS) cause acute poststreptococcal glomerulonephritis (APSGN), including M types 1, 2, 4, 12, 25, 49, 57, 59, 60, and 61 (5).

Although the prevalence of APSGN has decreased, the incidence in developing countries remains high (5). Several epidemics or outbreaks of APSGN have been reported in China in recent years, affecting the Zhejiang, Guangdong, and Fujian provinces (15, 16, 21, 31). A total of 119 cases of patients from ages 6 to 13 years were reported in four outbreaks, and two patients died. Most patients had a recent history of pharyngeal infection, 14 cases followed scarlet fever, and only 6 cases developed after streptococcal pyoderma. Despite the effects of APSGN, no further molecular biological information for nephritogenic streptococci isolated in China is currently available.

This study is focused on the molecular analysis of two distinct emm types of GAS isolates recovered from the throat cultures of patients with AGN and pharyngitis and from asymptomatic carriers during outbreaks of APSGN reported in Guizhou, China. The analysis, using pulsed-field gel electrophoresis (PFGE) and streptococcal pyrogenic exotoxin (spe) gene profiles, including the speA, speB, and speC genes, of outbreak isolates showed only minor variations.

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Sampling. In November 2005, an outbreak of AGN was reported in Guizhou Province, China, covering two adjacent counties, 11 townships, and several primary schools. From 4 to 14 November 2005, 62 cases with edema of the face or extremities were reported by the emergency public health events reporting system from Rongjiang County and Leishan County in Guizhou Province, and all of them were from three townships in the two counties. Patients were from 4 to 17 years of age, with an average age of 10 ± 3.3 years. All patients experienced a sudden onset of edema and had other symptoms, including weakness, fever, or abdominal pain. Over 30% (16/46) of patients had a history of upper respiratory infection 1 to 3 weeks before disease onset; 63.3% (31/49) of patients had reduced urine, microhematuria, or proteinuria; 63% (17/27) had raised antistreptolysin O titer; and 100% (6/6) had low C3 complement. Most patients received no treatment, edema was reduced in 1 week, and two patients died. In the following investigation, 37 schools in the three townships were stratified into three groups as epidemic, sporadic, and unaffected schools, by reported incidence of edema. Epidemic schools included Qiaolai School (19 cases and attack rate of 7.2%) in Sanjiang Township of Rongjiang County, and Kaitun School (20 cases and attack rate of 11.8%) in Yongle Township of Leishan County. Sporadic schools included four primary schools of Rongjiang County, with the case rates from 0.93% to 5.2%, and three schools were randomly selected for the study. Three of 31 unaffected schools were randomly selected as controls, 2 of which are located in Rongjiang County and 1 located in Leishan County. A total of 368 throat swabs and serum samples were collected from children. Determination of antistreptolysin O levels in serum was performed in Beijing Children's Hospital affiliated to Capital Medical University (unpublished data). It should be noted that there was no GAS isolated from children in the unaffected school of Leishan County, so unaffected schools included in the present study were only in Rongjiang County.

Source of GAS strains. A total of 68 GAS isolates were recovered from 368 throat swabs. Among them, 23 isolates were recovered from the AGN patients (28.0%), 7 were isolated from the pharyngitis patients (53.8%), and 38 were isolated from the carriers (13.9%). All isolates showed beta-hemolysis on Trypticase soy agar including 5% sheep blood, which tested negative in the catalase test; were susceptible to 0.04 U of bacitracin; and were Lancefield grouped as GAS using a streptococcal grouping kit (BioMérieux, France). All isolates were stored at –70°C in brain heart infusion broth containing 15% glycerol before laboratory operation.

Genotyping. Analysis of emm typing, PFGE, multilocus sequence typing (MLST), and sof sequence typing was performed as previously described (1, 3, 8; http://www.cdc.gov/ncidod/biotech/strep/M-ProteinGene_typing.htm). For emm typing, the sequence of the first 240 bases obtained was submitted to the National Centers for Disease Control Biotechnology Core Facility Computing Laboratory, and emm type and subtype were determined by the new parameters for assigning types and subtypes described in the Centers for Disease Control and Prevention (CDC) sequence database (http://www.cdc.gov/ncidod/biotech/strep/M-ProteinGene_typing.htm). All isolates were subjected to emm typing, and isolates of outbreak types were analyzed by PFGE and sof gene amplification. The digital PFGE patterns were analyzed with BioNumerics software (Applied Maths, Kortrijk, Belgium). At least one isolate from each PFGE pattern was further analyzed by MLST and sof gene sequence typing. The multilocus sequence data were analyzed using eBURST (10).

Detection of speA, speB, and speC genes by PCR. All isolates of the two outbreak types were analyzed for amplification of speA, speB, and speC genes using the primers speA-fw (5'-ACT TAA GAA CCA AGA GAT GG-3') and speA-rev (5'-CTT TAT TCT TAG GTA TGA AC-3'), speB-fw (5'-GTC AAC ATG CAG CTA CAG GA-3') and speB-rev (5'-AAT ACC AAC ATC AGC CAT CA-3'), and speC-fw (5'-TCT AGT CCC TTC ATT TGG TG-3') and speC-rev (5'-GTA AAT TTT TCA ACG ACA CA-3'), respectively, as reported previously (11, 30). The PCR cycle used for amplification was as follows: denaturation at 94°C for 15 s, annealing at 55°C for 30 s, extension at 72°C for 1 min for 30 cycles, and a final extension at 72°C for 5 min. Each reaction was preceded by a single denaturation at 94°C for 5 min. GAS strain ATCC 700294 was used as a positive control.

Susceptibility tests. Susceptibility to ampicillin, ceftriaxone, vancomycin, erythromycin, tetracycline, levofloxacin, chloramphenicol, and clindamycin was assessed by Etest (AB Biodisk, Solna, Sweden). All results were interpreted according to Clinical and Laboratory Standards Institute criteria (4). The following breakpoints for susceptibility were used: ampicillin, 0.25 µg/ml; ceftriaxone, 0.5 µg/ml; vancomycin, 1 µg/ml; erythromycin, 0.25 µg/ml; tetracycline, 2 µg/ml; levofloxacin, 2 µg/ml; chloramphenicol, 4 µg/ml; and clindamycin, 0.25 µg/ml. The resistance breakpoints used in this study were as follows: erythromycin, 1 µg/ml; tetracycline, 8 µg/ml; levofloxacin, 8 µg/ml; chloramphenicol, 16 µg/ml; and clindamycin, 1 µg/ml. Streptococcus pneumoniae strain ATCC 49619 was used as a quality control.

Nucleotide sequence accession number. The emm gene sequences of new subtypes described in the present study can be found in GenBank with the following accession numbers: EF489042 (emm114.6), EF489043 (st106m.2), EF494746 (emm1.4), and EF494746 (st106m.4).

Statistical analysis. Chi-square analysis was used to assess the differences of emm type distributions between AGN patients and asymptomatic carriers. A P value of 0.05 was considered to be significant.

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emm type analysis. A total of 11 different emm/st types were identified among the 68 GAS isolates (Table 1). Of these, 65 (95.6%) isolates belonged to 10 emm types that refer to type-specific sequences of one of the standard reference GAS strains, and 3 (4.4%) belonged to one sequence type (st) that has not yet been validated by international committee. Five isolates (7.4%) had new subtype sequences belonging to 3 emm/st types. Table 2 shows the characteristics of new subtype sequences detected in the present study. These new subtypes had point mutations or deletions in the hypervariable N-terminal 50 residues compared with the sequences of each reference strain.

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TABLE 1. Distribution of emm types in different populations

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TABLE 2. Allelic variations detected in this study

The predominant types identified were emm12, emm60, emm63, and emm95, which constituted 83.8% of all isolates. The other emm/st types identified in this study were emm1, emm4, emm22, emm58, emm113, emm114, and st106m, each of which was detected in only one or two isolates.

Among 23 GAS isolates from AGN patients, six different emm/st types were found (Table 1): emm12, emm58, emm60, emm63, emm95, and st106m.2. Only three emm/st types were identified in isolates from patients with pharyngitis: emm60, emm95, and st160m. A total of 10 distinct emm/st types were detected in 38 isolates from asymptomatic carriers: emm1, emm4, emm12, emm22, emm60, emm63, emm95, emm113, emm114, and st106m (Table 1). emm60 and emm63 were the most prevalent types in isolates from both AGN patients and asymptomatic carriers, and distributions of the two types were not significantly different between the two groups (P > 0.05) (Table 1).

Distributions of emm types were entirely different between the two counties studied, with no common emm types observed in the two groups (Table 3). Among 51 GAS isolates from Rongjiang County, seven emm types were identified: emm4, emm12, emm22, emm60, emm95, emm113, and st106m. Of these, emm60 was the predominant type, constituting 64.7% (33/51). Only four emm types—emm1, emm58, emm63, and emm114—were identified in 17 GAS isolates from Leishan County, and emm63 (n = 13, 76.5%) was the most prevalent type.

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TABLE 3. Distribution of emm types in the counties

In one of the two epidemic schools, Qiaolai School (Rongjiang County), the most prevalent type was emm60 (n = 16, 64%), followed by emm12 (n = 3, 12%) and emm22 (n = 2, 8%) (Table 4), which constituted 80% and 75% of isolates from AGN and pharyngitis patients, respectively, and nearly half of asymptomatic carriers (46.5%). In the other school, Kaitun School (Leishan County), emm63 constituted 77.8% and 75% among AGN and asymptomatic carriers, respectively (Table 4). Interestingly, despite being the most prevalent type among children of Rongjiang County or Qiaolai School, as well as in all of the children studied, emm60 was not detected in Kaitun School. In sporadic and unaffected schools, distribution of emm types was similar to that in Qiaolai School (data not shown).

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TABLE 4. Distribution of emm types in the two epidemic schools

Genetic characteristics of outbreak strains. A total of 46 isolates identified as emm60 and emm63 were further analyzed by PFGE (Fig. 1). Among 33 isolates of emm60, 31 shared an indistinguishable pattern (SPYS16C0001). There were also two other patterns detected in emm60 isolates, named SPYS16C0002 and SPYS16C0003, which had only one or two band differences from SPYS16C0001. Each of the two patterns was detected in one isolate from a patient with AGN or pharyngitis. Two PFGE patterns (SPYS16C0004 and SPYS16C0005) were identified in 13 isolates of emm63, with two band differences between them. SPYS16C0004 was the predominant pattern shared by 12 isolates, and SPYS16C0005 was identified in one isolate from a carrier.

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FIG. 1. PFGE profiles and background of 46 GAS isolates of the two outbreak types. The dendrogram was constructed with BioNumerics software, with a 1.5% position tolerance and 1% optimization by using the unweighted paired group with arithmetic averaging algorithm and Dice similarity coefficients. Two clusters were obtained with similarity coefficients greater than 85%, containing isolates of emm60 and emm63.

At least one representative of each PFGE pattern was selected to obtain the allelic profiles of seven housekeeping gene loci for MLST analysis. Isolates of emm60 and emm63 that were investigated were identified as MLST sequence type 53 (ST53) and ST426, respectively. ST426 was a new allelic profile identified in this study. To obtain genetic relationships of outbreak strains with isolates from various origins, the allelic profiles in the Streptococcus pyogenes MLST database (http://spyogenes.mlst.net) were analyzed with eBURST, an algorithm that can divide MLST data into groups of related isolates and clonal complexes by the level of similarity of their allelic profiles (10). A population snapshot including 380 STs available in the MLST database (accessed 18 March 2008) was generated by setting the group definition of seven shared alleles to zero, as described previously (18) (data not shown). Fifty-five clonal complexes were observed by eBURST, and a founder ST was assigned in 26 of 55 clonal complexes. However, there was no single-locus variant of ST53 or ST426 observed in the MLST database.

PCR amplification for the sof, speA, speB, and speC genes was conducted for the isolates of emm60 and emm63. The genes sof and speB were detected in all isolates. But the occurrences of speA and speC were different between the two types. emm60 isolates were PCR negative for the two virulence genes, while emm63 isolates were positive for the two genes, except one sample from an asymptomatic carrier, which was PCR negative for the speA gene. sof gene sequences of emm60 and emm63 were further identified as sof60 and sof63, respectively.

Antimicrobial susceptibility. Among 68 GAS isolates, 88.2% and 97.1% were resistant to erythromycin and tetracycline, respectively (Table 5). One isolate showed intermediate resistance to chloramphenicol, three isolates were resistant to clindamycin, and isolates resistant to ampicillin, ceftriaxone, vancomycin, or levofloxacin were never detected. The resistance rates of emm60 and emm63 isolates to erythromycin and tetracycline were both 100%.

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TABLE 5. Susceptibility of 68 GAS isolates to antibiotics

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As a result of an early epidemiological study of hospitalized patients in China, the percentage of AGN in the patients with urinary system diseases was reduced from 53% in 1982 to 37% in 1992 (33). Nevertheless, there still have been epidemics or even outbreaks of AGN reported in China in recent years (15, 16, 21, 31).

In this study, 68 GAS isolates were recovered from throat cultures of patients with AGN and pharyngitis and from asymptomatic carriers during outbreaks of AGN in Guizhou Province, China. The GAS samples were first analyzed by emm typing in order to investigate the genetic profiles of nephritogenic GAS in China. A total of 11 different emm/st types were identified. Only three isolates were identified as st type, while the rest were emm types within the sequence of emm1 to emm124 typically encountered during investigations in other countries (9, 14, 25, 27, 28). These data are consistent with the prediction that most existing emm types within GAS have already been documented throughout the world, as described previously (25).

The types of GAS infecting the children during the outbreak were completely different between the two counties studied, in spite of their geographic linkage. The most frequent types in Rongjiang County and Leishan County were emm60 and emm63, respectively. Geographical differences of prevalent emm types between the two counties may be due to the mountains between them, which function as a physical barrier that prevents the transfer of GAS strains between the two populations. Comparison of emm type distributions between the two epidemic schools further determined emm60 and emm63 as the cause of AGN outbreaks, since emm60 was detected in 80% of isolates from AGN patients of Qiaolai School and emm63 was detected in 77.8% of isolates from AGN patients of Kaitun School. Other emm types identified in AGN patients were detected in no more than two isolates and thus were identified as sporadic cases.

Genetic characteristics of outbreak strains with two emm sequence types (emm60 and emm63) were further analyzed by PFGE and MLST. Isolates of each emm type were genetically identical or closely related according to the criteria for interpreting PFGE patterns proposed by Tenover et al. (29) and identified as ST53 (emm60) and ST426 (emm63) by MLST analysis. The population structures of GAS isolates available in the MLST database (18 March 2008), including those of STs detected in this study, showed few clonal complexes and identified ST53 and ST426 as singletons (data not shown). ST426 was identified for the first time in this study, and ST53 has been found in the United States and Poland. The ST53 isolate found in the United States was also recovered from an AGN patient, indicating that ST53 is a nephritogenic clone.

Outbreak strains of emm60 and emm63 were sof positive, and the sequences of the sof gene were identified as sof60 and sof63, respectively, which is consistent with the background of the reference strains of each type available in the CDC emm database of GAS (see above). The virulence genes speA, speB, and speC were amplified from outbreak strains. All isolates from each emm type had the same spe gene profiles, except for one isolate of emm63. It has been suggested in previous studies that pyrogenic exotoxins functioning as superantigens potentially play a role in the pathogenesis of APSGN (32). However, the differences of spe gene profiles between emm60 and emm63 indicated that SpeA and SpeC may be unnecessary for the initiation of APSGN. There have been other superantigens discovered recently, including SpeF (20), SpeG (24), SpeH (24), SpeI (23), SpeJ (17), streptococcal superantigen (19), and streptococcal mitogenic exotoxin (SmeZ) (13), indicating that various superantigens expressed by different GAS isolates may play a role in the pathogenesis of APSGN.

GAS type M60, also known as nephritogenic streptococci, was first reported in Alabama as early as 1965 (6), and it caused epidemic nephritis in Trinidad in 1968 and 1969 (22). According to information from the CDC emm database (see above), the reference strain of the emm60.1 subtype was originally identified in Malaysia and then found in Brazil and Poland. However, there have been no previous reports of nephritogenic GAS of type emm60 identified in China.

The reference strain of emm63.0 was originally identified in England and then found in the United States, Brazil, Egypt, and Nepal as throat or skin isolates (as reported in the CDC database) and also in China (12). However, its association with AGN was unknown until we reported in this study results indicating an AGN outbreak caused by M63.

The emm types prevalent in China were mainly emm1, emm12, and emm18 (2, 12). Of these, emm1 and emm12 were also identified in the present study. emm12 constituted 22.7% of sporadic strains (those samples without isolates of emm60 and emm63), thus making emm12 another prevalent strain among the children investigated. Other emm types identified in this study, including emm22, emm60, emm95, emm113, and emm114, had never been isolated previously in China.

The resistance of GAS to erythromycin, tetracycline, and clindamycin is particularly serious in China, and it is strongly related to the misuse and overuse of antibiotics in hospitals and communities. In the 1990s, the erythromycin resistance rate in Beijing was reported as 66.7% (26), and the results of antibiotic resistance analysis of GAS isolates from the Jilin, Hubei, Sichuan, and Guangdong provinces showed that overall rates of GAS resistance to erythromycin, tetracycline, and clindamycin were 43.3%, 65.7%, and 34%, respectively (7). Jilin Province showed the highest rates of resistance to erythromycin (79.4%), tetracycline (94.8%), and clindamycin (84.5%). Hubei Province had the lowest rate of erythromycin resistance (17.8%), and urban areas of Guangzhou in Guangdong Province had the lowest resistance rates of tetracycline (34.6%) and clindamycin (5.8%). As shown in a recent epidemiological study of GAS isolates in China, resistance rates of GAS to erythromycin, tetracycline, and clindamycin were as high as 91.8%, 93.4%, and 80%, respectively, which were higher than reported rates in other countries (12).

In this study, overall rates of erythromycin and tetracycline resistance were 88.2% and 97.1%, respectively, which is consistent with the current status of antibiotic resistance of GAS in China. Outbreak strains of the two emm types were observed to be multiresistant to erythromycin and tetracycline. However, only three isolates were identified to be resistant to clindamycin in the present study.

This study has demonstrated that two distinct emm types (emm60 and emm63) are responsible for two outbreaks of APSGN in southern China. Outbreak strains of each type were sof positive, shared genetic characteristics and spe gene profiles (speA, speB, and speC), and were resistant to erythromycin and tetracycline.

 
This work was supported by a fund for disease control from the National Institute for Communicable Disease Control and Prevention.

We appreciate our colleagues Yi-xin Gu, Yuan-hai You, Yuan Hu, Qing-hua Zou, Jing Li, Chun-xiang Fan, Xiao-yun Ji, Hui-fang Zhang, and Yuan-yuan Jiang for their excellent technical assistance.

 
* Corresponding author. Mailing address for Jian-zhong Zhang: National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, P.O. Box 5, Changping, Beijing 102206, People's Republic of China. Phone and fax: 86-10-61739456. E-mail: helico99{at}sina.com. Mailing address for Zi-jun Wang: Office of Disease Control and Emergency Response, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China. Phone: 86-13-910751827. Fax: 86-10-63152572. E-mail: wangzj{at}chinacdc.cn

Published ahead of print on 30 December 2008.

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Journal of Clinical Microbiology, March 2009, p. 715-720, Vol. 47, No. 3
0095-1137/09/$08.00+0     doi:10.1128/JCM.00747-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

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