Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study

Hongwei Zhou; Siheng Wang; Yuchen Wu; Ning Dong; Xiaoyang Ju; Chang Cai; Ruichao Li; Yan Li; Congcong Liu; Jiayue Lu; Edward Wai-Chi Chan; Sheng Chen; Rong Zhang; Zhangqi Shen

doi:10.1016/j.ijantimicag.2022.106645

Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study

Hongwei Zhou (Co-first Author), Siheng Wang (Co-first Author), Yuchen Wu, Ning Dong, Xiaoyang Ju, Chang Cai, Ruichao Li, Yan Li, Congcong Liu, Jiayue Lu, Edward Wai-Chi Chan, Sheng Chen^*, Rong Zhang, Zhangqi Shen^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

18 Citations (Scopus)

Abstract

Objectives: Enterobacter cloacae complex (ECC) is among the most common carbapenem-resistant Enterobacteriaceae (CRE) in China. The emergence of mcr has rendered CRE strains resistant to the last-line antibiotic colistin. This study investigated the prevalence of mcr-9 and mcr-10 in carbapenem-resistant ECC (CRECC) and carbapenem-susceptible ECC (CSECC) in China.

Methods: The CRECC and CSECC strains were collected from different regions of China. Antimicrobial susceptibility tests, conjugation experiments, whole genome sequencing, bioinformatic analysis, and quantitative RT-PCR were performed to understand the mechanisms of resistance and transmission of mcr in ECC.

Results: A total of 534 ECC were collected, among which 57 (10.7%) and 23 (4.3%) were positive for mcr-9 and mcr-10, respectively. The prevalence of mcr-9 in CRECC was significantly higher than that in CSECC (31.8% vs. 3.7%; P < 0.001), while the prevalence of mcr-10 in CRECC was significantly lower (0.8% vs. 5.5%; P < 0.05). Most mcr-9-positive strains (n = 45, 78.9%) exhibited multidrug-resistant phenotype, and four (17.4%) of the mcr-10-positive strains exhibited multi-drug resistance. Coexistence of mcr and carbapenemase genes was commonly observed, including 41 (71.9%) mcr-9-positive strains and one (4.3%) mcr-10-positive strain, and the possibility of co-transfer was confirmed by conjugation experiments. The mcr-positive ECC were highly diverse, while most mcr genes were plasmid-encoded, indicating the important role of plasmids in the transmission of mcr in ECC. Furthermore, the expression of mcr-9 was increased after induction by colistin.

Conclusions: The widespread mcr genes and co-transfer with carbapenemase genes among ECC strains pose an urgent threat to public health.

Original language	English
Article number	106645
Journal	International Journal of Antimicrobial Agents
Volume	60
Issue number	4
Online published	28 Jul 2022
DOIs	https://doi.org/10.1016/j.ijantimicag.2022.106645
Publication status	Published - Oct 2022

Funding

This work was supported by the National Natural Science Foundation of China [grant numbers 81861138052, 22193064, 32141001]; Guangdong Major Project of Basic and Applied Basic Research [grant number 2020B0301030005]; and NSFC/RGC grant [grant number NSFC-RGC, N_PolyU521/18] from the National Natural Science Fund in China and Research Grant Council of the Government of Hong Kong SAR.

Research Keywords

mcr-9
mcr-10
Enterobacter cloacae complex
Colistin
Carbapenem-resistant Enterobacteriaceae
Epidemiology

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RGC-funded

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Zhou, H., Wang, S., Wu, Y., Dong, N., Ju, X., Cai, C., Li, R., Li, Y., Liu, C., Lu, J., Chan, E. W.-C., Chen, S., Zhang, R., & Shen, Z. (2022). Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study. International Journal of Antimicrobial Agents, 60(4), Article 106645. https://doi.org/10.1016/j.ijantimicag.2022.106645

@article{2ff44494f235463faee97a7c860d399e,

title = "Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study",

abstract = "Objectives: Enterobacter cloacae complex (ECC) is among the most common carbapenem-resistant Enterobacteriaceae (CRE) in China. The emergence of mcr has rendered CRE strains resistant to the last-line antibiotic colistin. This study investigated the prevalence of mcr-9 and mcr-10 in carbapenem-resistant ECC (CRECC) and carbapenem-susceptible ECC (CSECC) in China.Methods: The CRECC and CSECC strains were collected from different regions of China. Antimicrobial susceptibility tests, conjugation experiments, whole genome sequencing, bioinformatic analysis, and quantitative RT-PCR were performed to understand the mechanisms of resistance and transmission of mcr in ECC.Results: A total of 534 ECC were collected, among which 57 (10.7%) and 23 (4.3%) were positive for mcr-9 and mcr-10, respectively. The prevalence of mcr-9 in CRECC was significantly higher than that in CSECC (31.8% vs. 3.7%; P < 0.001), while the prevalence of mcr-10 in CRECC was significantly lower (0.8% vs. 5.5%; P < 0.05). Most mcr-9-positive strains (n = 45, 78.9%) exhibited multidrug-resistant phenotype, and four (17.4%) of the mcr-10-positive strains exhibited multi-drug resistance. Coexistence of mcr and carbapenemase genes was commonly observed, including 41 (71.9%) mcr-9-positive strains and one (4.3%) mcr-10-positive strain, and the possibility of co-transfer was confirmed by conjugation experiments. The mcr-positive ECC were highly diverse, while most mcr genes were plasmid-encoded, indicating the important role of plasmids in the transmission of mcr in ECC. Furthermore, the expression of mcr-9 was increased after induction by colistin.Conclusions: The widespread mcr genes and co-transfer with carbapenemase genes among ECC strains pose an urgent threat to public health.",

keywords = "mcr-9, mcr-10, Enterobacter cloacae complex, Colistin, Carbapenem-resistant Enterobacteriaceae, Epidemiology",

author = "Hongwei Zhou and Siheng Wang and Yuchen Wu and Ning Dong and Xiaoyang Ju and Chang Cai and Ruichao Li and Yan Li and Congcong Liu and Jiayue Lu and Chan, {Edward Wai-Chi} and Sheng Chen and Rong Zhang and Zhangqi Shen",

year = "2022",

month = oct,

doi = "10.1016/j.ijantimicag.2022.106645",

language = "English",

volume = "60",

journal = "International Journal of Antimicrobial Agents",

issn = "0924-8579",

publisher = "Elsevier B.V.",

number = "4",

}

Zhou, H, Wang, S, Wu, Y, Dong, N, Ju, X, Cai, C, Li, R, Li, Y, Liu, C, Lu, J, Chan, EW-C, Chen, S , Zhang, R & Shen, Z 2022, 'Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study', International Journal of Antimicrobial Agents, vol. 60, no. 4, 106645. https://doi.org/10.1016/j.ijantimicag.2022.106645

Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study. / Zhou, Hongwei (Co-first Author); Wang, Siheng (Co-first Author); Wu, Yuchen et al.
In: International Journal of Antimicrobial Agents, Vol. 60, No. 4, 106645, 10.2022.

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

TY - JOUR

T1 - Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China

T2 - a prevalence and molecular epidemiology study

AU - Zhou, Hongwei

AU - Wang, Siheng

AU - Wu, Yuchen

AU - Dong, Ning

AU - Ju, Xiaoyang

AU - Cai, Chang

AU - Li, Ruichao

AU - Li, Yan

AU - Liu, Congcong

AU - Lu, Jiayue

AU - Chan, Edward Wai-Chi

AU - Chen, Sheng

AU - Zhang, Rong

AU - Shen, Zhangqi

PY - 2022/10

Y1 - 2022/10

N2 - Objectives: Enterobacter cloacae complex (ECC) is among the most common carbapenem-resistant Enterobacteriaceae (CRE) in China. The emergence of mcr has rendered CRE strains resistant to the last-line antibiotic colistin. This study investigated the prevalence of mcr-9 and mcr-10 in carbapenem-resistant ECC (CRECC) and carbapenem-susceptible ECC (CSECC) in China.Methods: The CRECC and CSECC strains were collected from different regions of China. Antimicrobial susceptibility tests, conjugation experiments, whole genome sequencing, bioinformatic analysis, and quantitative RT-PCR were performed to understand the mechanisms of resistance and transmission of mcr in ECC.Results: A total of 534 ECC were collected, among which 57 (10.7%) and 23 (4.3%) were positive for mcr-9 and mcr-10, respectively. The prevalence of mcr-9 in CRECC was significantly higher than that in CSECC (31.8% vs. 3.7%; P < 0.001), while the prevalence of mcr-10 in CRECC was significantly lower (0.8% vs. 5.5%; P < 0.05). Most mcr-9-positive strains (n = 45, 78.9%) exhibited multidrug-resistant phenotype, and four (17.4%) of the mcr-10-positive strains exhibited multi-drug resistance. Coexistence of mcr and carbapenemase genes was commonly observed, including 41 (71.9%) mcr-9-positive strains and one (4.3%) mcr-10-positive strain, and the possibility of co-transfer was confirmed by conjugation experiments. The mcr-positive ECC were highly diverse, while most mcr genes were plasmid-encoded, indicating the important role of plasmids in the transmission of mcr in ECC. Furthermore, the expression of mcr-9 was increased after induction by colistin.Conclusions: The widespread mcr genes and co-transfer with carbapenemase genes among ECC strains pose an urgent threat to public health.

AB - Objectives: Enterobacter cloacae complex (ECC) is among the most common carbapenem-resistant Enterobacteriaceae (CRE) in China. The emergence of mcr has rendered CRE strains resistant to the last-line antibiotic colistin. This study investigated the prevalence of mcr-9 and mcr-10 in carbapenem-resistant ECC (CRECC) and carbapenem-susceptible ECC (CSECC) in China.Methods: The CRECC and CSECC strains were collected from different regions of China. Antimicrobial susceptibility tests, conjugation experiments, whole genome sequencing, bioinformatic analysis, and quantitative RT-PCR were performed to understand the mechanisms of resistance and transmission of mcr in ECC.Results: A total of 534 ECC were collected, among which 57 (10.7%) and 23 (4.3%) were positive for mcr-9 and mcr-10, respectively. The prevalence of mcr-9 in CRECC was significantly higher than that in CSECC (31.8% vs. 3.7%; P < 0.001), while the prevalence of mcr-10 in CRECC was significantly lower (0.8% vs. 5.5%; P < 0.05). Most mcr-9-positive strains (n = 45, 78.9%) exhibited multidrug-resistant phenotype, and four (17.4%) of the mcr-10-positive strains exhibited multi-drug resistance. Coexistence of mcr and carbapenemase genes was commonly observed, including 41 (71.9%) mcr-9-positive strains and one (4.3%) mcr-10-positive strain, and the possibility of co-transfer was confirmed by conjugation experiments. The mcr-positive ECC were highly diverse, while most mcr genes were plasmid-encoded, indicating the important role of plasmids in the transmission of mcr in ECC. Furthermore, the expression of mcr-9 was increased after induction by colistin.Conclusions: The widespread mcr genes and co-transfer with carbapenemase genes among ECC strains pose an urgent threat to public health.

KW - mcr-9

KW - mcr-10

KW - Enterobacter cloacae complex

KW - Colistin

KW - Carbapenem-resistant Enterobacteriaceae

KW - Epidemiology

UR - http://www.scopus.com/inward/record.url?scp=85138533554&partnerID=8YFLogxK

UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85138533554&origin=recordpage

U2 - 10.1016/j.ijantimicag.2022.106645

DO - 10.1016/j.ijantimicag.2022.106645

M3 - RGC 21 - Publication in refereed journal

C2 - 35907595

SN - 0924-8579

VL - 60

JO - International Journal of Antimicrobial Agents

JF - International Journal of Antimicrobial Agents

IS - 4

M1 - 106645

ER -

Carriage of the mcr-9 and mcr-10 genes in clinical strains of the Enterobacter cloacae complex in China: a prevalence and molecular epidemiology study

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