The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan
ABSTRACT The incidence of Elizabethkingia anophelis bacteremia increased significantly in a tertiary hospital, Changhua Christian Hospital (CCH) since 2013. The infection density was 1.3 and 8.1 cases per 100,000 patient-days between 2005 and 2012 and 2013 and 2020, respectively (P < 0.05). Durin...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01682-21 |
| _version_ | 1818323327914082304 |
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| author | Yu-Lin Lee Kuan-Ming Liu Hui-Lan Chang Yi-Ci Liao Jen-Shiou Lin Fang-Yen Kung Cheng-Mao Ho Kai-Hsiang Lin Ying-Tsong Chen |
| author_facet | Yu-Lin Lee Kuan-Ming Liu Hui-Lan Chang Yi-Ci Liao Jen-Shiou Lin Fang-Yen Kung Cheng-Mao Ho Kai-Hsiang Lin Ying-Tsong Chen |
| author_sort | Yu-Lin Lee |
| collection | DOAJ |
| description | ABSTRACT The incidence of Elizabethkingia anophelis bacteremia increased significantly in a tertiary hospital, Changhua Christian Hospital (CCH) since 2013. The infection density was 1.3 and 8.1 cases per 100,000 patient-days between 2005 and 2012 and 2013 and 2020, respectively (P < 0.05). During an outbreak investigation, a specific lineage of E. anophelis strains was identified by the pulsed-field gel electrophoresis analysis. To evaluate the evolution of the specific E. anophelis lineage, whole-genome sequencing was performed, and unique genomic features (GRs) were determined by comparative genomic analysis. The specific E. anophelis lineage was novel compared to worldwide strains ever reported by cg-MLST phylogenic and whole-genome comparative analysis. Multiplex PCR using primers designed from unique GRs were performed for prevalence screening among isolates from the CCH and nationwide isolates from the Taiwan surveillance of Antimicrobial Resistance (TSAR) Program. The proportion of the specific E. anophelis lineage increased from 7.9% (3/38) during 2005-2012 to 89.2% (223/250) during 2013-2020 (P < 0.05). Although E. anophelis usually confers resistance to multiple antibiotics with limited therapeutic options, the E. anophelis strains in the specific lineage had higher ciprofloxacin resistance (100% [226/226] versus 27.4% [17/62], P < 0.05) and was associated with a higher 14-day mortality rates (33.2% [37/226] versus 16.1% [10/62], P < 0.05) than other strains at CCH. A similarly increasing trend was also found in the national TSAR program during 2002-2018 (p for trend <0.05). We concluded that a novel lineage of E. anophelis strains has emerged dominantly in Taiwan. The genomic features are important for further investigations of epidemiology, resistance, virulence, and appropriate treatment. IMPORTANCE Elizabethkingia anophelis is an emerging multidrug resistant pathogen caused several global outbreaks recently. E. anophelis was frequently misidentified as E. meningoseptica in the past by conventional culture methods; therefore, the prevalence was often underestimated. Through revised identification, an increasing trend of E. anophelis infection was noted in a tertiary hospital and a dominant lineage of strains was recognized by genotyping. To our best knowledge, the dominant lineage of E. anophelis is novel in comparison to other worldwide strains by whole-genome comparative analysis and several unique genomic regions were found. The whole-genome sequencing data also demonstrated multiple putative virulence factors and genes associated with multidrug resistance. In our study, we identified a specially evolved E. anophelis in Taiwan with increasing nationwide dominance. This study will assist in further epidemiology surveillance and developing corresponsive infection control policies to restrain it potential of global dissemination. |
| first_indexed | 2024-12-13T11:10:56Z |
| format | Article |
| id | doaj.art-db7bd878480944e0bb8e088771b7a771 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-13T11:10:56Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-db7bd878480944e0bb8e088771b7a7712022-12-21T23:48:45ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-02-0110110.1128/spectrum.01682-21The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in TaiwanYu-Lin Lee0Kuan-Ming Liu1Hui-Lan Chang2Yi-Ci Liao3Jen-Shiou Lin4Fang-Yen Kung5Cheng-Mao Ho6Kai-Hsiang Lin7Ying-Tsong Chen8Department of Internal Medicine, Changhua Christian Hospital, Changhua County, TaiwanInstitute of Genomics and Bioinformatics, National Chung Hsing University, Taichung City, TaiwanDepartment of Internal Medicine, Changhua Christian Hospital, Changhua County, TaiwanInstitute of Genomics and Bioinformatics, National Chung Hsing University, Taichung City, TaiwanDepartment of Laboratory Medicine, Changhua Christian Hospital, Changhua County, TaiwanDepartment of Laboratory Medicine, Changhua Christian Hospital, Changhua County, TaiwanDepartment of Clinical Pathology and Laboratory Medicine, Taichung Tzu Chi Hospital, Taichung City, TaiwanDepartment of Clinical Pathology and Laboratory Medicine, Taichung Tzu Chi Hospital, Taichung City, TaiwanPh.D. Program in Medical Biotechnology, National Chung Hsing University, Taichung City, TaiwanABSTRACT The incidence of Elizabethkingia anophelis bacteremia increased significantly in a tertiary hospital, Changhua Christian Hospital (CCH) since 2013. The infection density was 1.3 and 8.1 cases per 100,000 patient-days between 2005 and 2012 and 2013 and 2020, respectively (P < 0.05). During an outbreak investigation, a specific lineage of E. anophelis strains was identified by the pulsed-field gel electrophoresis analysis. To evaluate the evolution of the specific E. anophelis lineage, whole-genome sequencing was performed, and unique genomic features (GRs) were determined by comparative genomic analysis. The specific E. anophelis lineage was novel compared to worldwide strains ever reported by cg-MLST phylogenic and whole-genome comparative analysis. Multiplex PCR using primers designed from unique GRs were performed for prevalence screening among isolates from the CCH and nationwide isolates from the Taiwan surveillance of Antimicrobial Resistance (TSAR) Program. The proportion of the specific E. anophelis lineage increased from 7.9% (3/38) during 2005-2012 to 89.2% (223/250) during 2013-2020 (P < 0.05). Although E. anophelis usually confers resistance to multiple antibiotics with limited therapeutic options, the E. anophelis strains in the specific lineage had higher ciprofloxacin resistance (100% [226/226] versus 27.4% [17/62], P < 0.05) and was associated with a higher 14-day mortality rates (33.2% [37/226] versus 16.1% [10/62], P < 0.05) than other strains at CCH. A similarly increasing trend was also found in the national TSAR program during 2002-2018 (p for trend <0.05). We concluded that a novel lineage of E. anophelis strains has emerged dominantly in Taiwan. The genomic features are important for further investigations of epidemiology, resistance, virulence, and appropriate treatment. IMPORTANCE Elizabethkingia anophelis is an emerging multidrug resistant pathogen caused several global outbreaks recently. E. anophelis was frequently misidentified as E. meningoseptica in the past by conventional culture methods; therefore, the prevalence was often underestimated. Through revised identification, an increasing trend of E. anophelis infection was noted in a tertiary hospital and a dominant lineage of strains was recognized by genotyping. To our best knowledge, the dominant lineage of E. anophelis is novel in comparison to other worldwide strains by whole-genome comparative analysis and several unique genomic regions were found. The whole-genome sequencing data also demonstrated multiple putative virulence factors and genes associated with multidrug resistance. In our study, we identified a specially evolved E. anophelis in Taiwan with increasing nationwide dominance. This study will assist in further epidemiology surveillance and developing corresponsive infection control policies to restrain it potential of global dissemination.https://journals.asm.org/doi/10.1128/spectrum.01682-21Elizabethkingia speciesmultidrug resistancenosocomial infectioncomparative genomics |
| spellingShingle | Yu-Lin Lee Kuan-Ming Liu Hui-Lan Chang Yi-Ci Liao Jen-Shiou Lin Fang-Yen Kung Cheng-Mao Ho Kai-Hsiang Lin Ying-Tsong Chen The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan Microbiology Spectrum Elizabethkingia species multidrug resistance nosocomial infection comparative genomics |
| title | The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan |
| title_full | The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan |
| title_fullStr | The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan |
| title_full_unstemmed | The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan |
| title_short | The Evolutionary Trend and Genomic Features of an Emerging Lineage of Elizabethkingia anophelis Strains in Taiwan |
| title_sort | evolutionary trend and genomic features of an emerging lineage of elizabethkingia anophelis strains in taiwan |
| topic | Elizabethkingia species multidrug resistance nosocomial infection comparative genomics |
| url | https://journals.asm.org/doi/10.1128/spectrum.01682-21 |
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