Association of the shuffling of Streptococcus pyogenes clones and the fluctuation of scarlet fever cases between 2000 and 2006 in central Taiwan

Abstract

Background: The number of scarlet fever occurrences reported between 2000 and 2006 fluctuated considerably in central Taiwan and throughout the nation. Isolates of Streptococcus pyogenes were collected from scarlet fever patients in central Taiwan and were characterized by emm sequencing and a standardized pulsed-field gel electrophoresis (PFGE) method. National weekly report data were collected for investigating epidemiological trends.

Results: A total of 23 emm types were identified in 1,218 S. pyogenes isolates. The five most prevalent emm types were emm12 (50.4%), emm4 (23.2%), emm1 (16.4%), emm6 (3.8%) and emm22 (3.0%). PFGE analysis with SmaI suggested that, with a few exceptions, strains with a common emm type belonged to the same clone. There were two large emm12 clones, one with DNA resistant to cleavage by SmaI. Each prevalent emm clone had major PFGE strain(s) and many minor strains. Most of the minor strains emerged in the population and disappeared soon after. Even some major strains remained prevalent for only 2-3 years before declining. The large fluctuation of scarlet fever cases between 2000 and 2006 was associated with the shuffling of six prevalent emm clones. In 2003, the dramatic drop in scarlet fever cases in central Taiwan and throughout the whole country was associated with the occurrence of a severe acute respiratory syndrome (SARS) outbreak that occurred between late-February and mid-June in Taiwan.

Conclusion: The occurrences of scarlet fever in central Taiwan in 2000-2006 were primarily caused by five emm types, which accounted for 96.8% of the isolates collected. Most of the S. pyogenes strains (as defined by PFGE genotypes) emerged and lasted for only a few years. The fluctuation in the number of scarlet fever cases during the seven years can be primarily attributed to the shuffling of six prevalent emm clones and to the SARS outbreak in 2003.

Figure 1

(A) Map of Taiwan and population density (B) National weekly reported cases of scarlet fever between 2000 and 2006. The total average throughout 2000–2006 is indicated by a red dashed line. The two stages of the SARS epidemic in 2003 are marked by blue (stage I) and red (stage II) bars.

Figure 2

Dendrogram constructed with PFGE-SmaI patterns, with their corresponding emm types and number of isolates obtained between 2000 and 2006. The clustering analysis was performed with BioNumerics using the UPGMA algorithm and the value of Dice predicted similarity of two patterns at settings of 1% optimization and 0.7% position tolerance.

Figure 3

Dendrogram constructed with PFGE-SgrAI patterns, with their corresponding emm types and number of isolates. DNA from these isolates was resistant to SmaI digestion. The clustering analysis was performed with BioNumerics using the UPGMA algorithm and the value of Dice predicted similarity of two patterns at settings of 1% optimization and 0.7% position tolerance.

Figure 4

Distribution of emm clones between 2000 and 2006. The number of Streptococcus pyogenes isolates analyzed is adjusted according to the number of adjusted annual confirmed of cases.