Volume 41 Issue 5
Sep.  2020
Turn off MathJax
Article Contents
Yu-Ping Cao, Qing-Qing Lin, Wan-Yun He, Jing Wang, Meng-Ying Yi, Lu-Chao Lv, Jun Yang, Jian-Hua Liu, Jian-Ying Guo. Co-selection may explain the unexpectedly high prevalence of plasmid-mediated colistin resistance gene mcr-1 in a Chinese broiler farm. Zoological Research, 2020, 41(5): 569-575. doi: 10.24272/j.issn.2095-8137.2020.131
Citation: Yu-Ping Cao, Qing-Qing Lin, Wan-Yun He, Jing Wang, Meng-Ying Yi, Lu-Chao Lv, Jun Yang, Jian-Hua Liu, Jian-Ying Guo. Co-selection may explain the unexpectedly high prevalence of plasmid-mediated colistin resistance gene mcr-1 in a Chinese broiler farm. Zoological Research, 2020, 41(5): 569-575. doi: 10.24272/j.issn.2095-8137.2020.131

Co-selection may explain the unexpectedly high prevalence of plasmid-mediated colistin resistance gene mcr-1 in a Chinese broiler farm

doi: 10.24272/j.issn.2095-8137.2020.131
#Authors contributed equally to this work
Funds:  This work was supported in part by the National Natural Science Foundation of China (31830099, 31902322), International Science and Technology Cooperation Project of Xinjiang Production and Construction Corps(XPCC) (2019BC004), Guangdong Special Support Program Innovation Team (2019BT02N054), and Innovation Team Project of Guangdong University (2019KCXTD001)
More Information
  • Corresponding author: E-mail: jhliu@scau.edu.cnjyguo@scau.edu.cn
  • Received Date: 2020-05-30
  • Accepted Date: 2020-07-21
  • Published Online: 2020-07-31
  • Publish Date: 2020-09-18
  • The rise of the plasmid-encoded colistin resistance gene mcr-1 is a major concern globally. Here, during a routine surveillance, an unexpectedly high prevalence of Escherichia coli with reduced susceptibility to colistin (69.9%) was observed in a Chinese broiler farm. Fifty-three (63.9%) E. coli isolates were positive for mcr-1. All identified mcr-1-positive E. coli (MCREC) were multidrug resistant and carried other clinically significant resistance genes. Furthermore, the mcr-1 genes were mainly located on the IncI2 and IncHI2 plasmids. Conjugation experiments unraveled the co-transfer of mcr-1 with other antibiotic resistance genes (blaCTX-M-55, blaCTX-M-14, floR, and fosA3) via the IncI2 (n=3) and IncHI2 (n=4) plasmids. The stable genetic context mcr-1-pap2 was common in the IncI2 plasmids, whereas ISApl1-mcr-1-pap2-ISApl1 was mainly found in the IncHI2 plasmids. The dominance of mcr-1-bearing IncI2 and IncHI2 plasmids and co-selection of mcr-1 with other antimicrobial resistance genes might contribute to the exceptionally high prevalence of mcr-1 in this broiler farm. Our results emphasized the importance of appropriate antibiotic use in animal production.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Barton BM, Harding GP, Zuccarelli AJ. 1995. A general method for detecting and sizing large plasmids. Analytical Biochemistry, 226(2): 235−240. doi: 10.1006/abio.1995.1220
    Casal J, Mateu E, Mejia W, Martin M. 2007. Factors associated with routine mass antimicrobial usage in fattening pig units in a high pig-density area. Veterinary Research, 38(3): 481−492. doi: 10.1051/vetres:2007010
    Elbediwi M, Li Y, Paudyal N, Pan H, Li XL, Xie SH, Rajkovic A, Feng YJ, Fang WH, Rankin SC, Yue M. 2019. Global burden of colistin-resistant bacteria: mobilized colistin resistance genes study (1980-2018). Microorganisms, 7(10): 461. doi: 10.3390/microorganisms7100461
    Falagas ME, Kastoris AC, Kapaskelis AM, Karageorgopoulos DE. 2010. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum β-lactamase producing, Enterobacteriaceae infections: a systematic review. The Lancet Infectious Diseases, 10(1): 43−50. doi: 10.1016/S1473-3099(09)70325-1
    Feng CY, Wen PP, Xu H, Chi XH, Li S, Yu X, Lin XM, Wu SQ, Zheng BW. 2019. Emergence and comparative genomics analysis of extended-spectrum-β-lactamase-producing Escherichia coli carrying mcr-1 in Fennec Fox imported from Sudan to China. mSphere, 4(6): e00732-19. doi: 10.1128/mSphere.00732-19
    Gautom RK. 1997. Rapid pulsed-field gel electrophoresis protocol for typing of Escherichia coli O157:H7 and other gram-negative organisms in 1 day. Journal of Clinical Microbiology, 35(11): 2977−2980. doi: 10.1128/JCM.35.11.2977-2980.1997
    Huang X, Yu L, Chen X, Zhi C, Yao X, Liu Y, Wu S, Guo Z, Yi L, Zeng Z, Liu JH. 2017. High prevalence of colistin resistance and mcr-1 Gene in Escherichia coli isolated from food animals in China. Frontiers in Microbiology, 8: 562.
    Lei T, Zhang JM, Jiang FF, He M, Zeng HY, Chen MT, Wu S, Wang J, Ding Y, Wu QP. 2019. First detection of the plasmid-mediated colistin resistance gene mcr-1 in virulent Vibrio parahaemolyticus. International Journal of Food Microbiology, 308: 108290. doi: 10.1016/j.ijfoodmicro.2019.108290
    Lentz SA, De Lima-Morales D, Cuppertino VM, Nunes LDS, Da Motta AS, Zavascki AP, Barth AL, Martins AF. 2016. Letter to the editor: Escherichia coli harbouring mcr-1 gene isolated from poultry not exposed to polymyxins in Brazil. Euro Surveillance, 21(26): 30267. doi: 10.2807/1560-7917.ES.2016.21.26.30267
    Li RC, Xie MM, Zhang JF, Yang ZQ, Liu LZ, Liu XB, Zheng ZW, Chan EWC, Chen S. 2017. Genetic characterization of mcr-1-bearing plasmids to depict molecular mechanisms underlying dissemination of the colistin resistance determinant. Journal of Antimicrobial Chemotherapy, 72(2): 393−401. doi: 10.1093/jac/dkw411
    Li ZK, Cao YP, Yi LX, Liu JH, Yang QW. 2019. Emergent polymyxin resistance: end of an Era?. Open Forum Infectious Diseases, 6(10): ofz368. doi: 10.1093/ofid/ofz368
    Ling ZR, Yin WJ, Shen ZQ, Wang Y, Shen JZ, Walsh TR. 2020. Epidemiology of mobile colistin resistance genes mcr-1 to mcr-9. Journal of Antimicrobial Chemotherapy. doi: 10.1093/jac/dkaa205.
    Liu LP, He DD, Lv LC, Liu WL, Chen XJ, Zeng ZL, Partridge SR, Liu JH. 2015. blaCTX-M-1/9/1 hybrid genes may have been generated from blaCTX-M-15 on an IncI2 plasmid. Antimicrobial Agents and Chemotherapy, 59(8): 4464−4470. doi: 10.1128/AAC.00501-15
    Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian GB, Dong BL, Huang XH, Yu LF, Gu DX, Ren HW, Chen XJ, Lv LC, He DD, Zhou HW, Liang ZS, Liu JH, Shen JZ. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. The Lancet Infectious Diseases, 16(2): 161−168. doi: 10.1016/S1473-3099(15)00424-7
    Liu YY, Liu JH. 2018. Monitoring colistin resistance in food animals, an urgent threat. Expert Review of Anti-infective Therapy, 16(6): 443−446. doi: 10.1080/14787210.2018.1481749
    Lv LC, Partridge SR, He LY, Zeng ZL, He DD, Ye JH, Liu JH. 2013. Genetic characterization of IncI2 plasmids carrying blaCTX-M-55 spreading in both pets and food animals in China. Antimicrobial Agents and Chemotherapy, 57(6): 2824−2827. doi: 10.1128/AAC.02155-12
    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18(3): 268−281. doi: 10.1111/j.1469-0691.2011.03570.x
    Migura-Garcia L, González-López JJ, Martinez-Urtaza J, Aguirre Sánchez JR, Moreno-Mingorance A, Perez De Rozas A, Höfle U, Ramiro Y, Gonzalez-Escalona N. 2020. mcr-colistin resistance genes mobilized by IncX4, IncHI2, and IncI2 plasmids in Escherichia coli of pigs and White Stork in Spain. Frontiers in Microbiology, 10: 3072. doi: 10.3389/fmicb.2019.03072
    Moawad AA, Hotzel H, Neubauer H, Ehricht R, Monecke S, Tomaso H, Hafez HM, Roesler U, El-Adawy H. 2018. Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli. Gut Pathogens, 10(1): 39. doi: 10.1186/s13099-018-0266-5
    Nang SC, Li J, Velkov T. 2019. The rise and spread of mcr plasmid-mediated polymyxin resistance. Critical Reviews in Microbiology, 45(2): 131−161. doi: 10.1080/1040841X.2018.1492902
    Nation RL, Li J. 2009. Colistin in the 21st century. Current Opinion in Infectious Diseases, 22(6): 535−543. doi: 10.1097/QCO.0b013e328332e672
    Perreten V, Strauss C, Collaud A, Gerber D. 2016. Colistin resistance gene mcr-1 in avian-pathogenic Escherichia coli in South Africa. Antimicrobial Agents and Chemotherapy, 60(7): 4414−4415. doi: 10.1128/AAC.00548-16
    Perrin-Guyomard A, Bruneau M, Houée P, Deleurme K, Legrandois P, Poirier C, Soumet C, Sanders P. 2016. Prevalence of mcr-1 in commensal Escherichia coli from French livestock, 2007 to 2014. Euro Surveillance, 21(6). doi: 10.2807/1560-7917.ES.2016.21.6.30135
    Quan JJ, Li X, Chen Y, Jiang Y, Zhou ZH, Zhang HC, Sun L, Ruan Z, Feng Y, Akova M, Yu YS. 2017. Prevalence of mcr-1 in Escherichia coli and Klebsiella pneumoniae recovered from bloodstream infections in China: a multicentre longitudinal study. The Lancet Infectious Diseases, 17(4): 400−410. doi: 10.1016/S1473-3099(16)30528-X
    Shen ZQ, Wang Y, Shen YB, Shen JZ, Wu CM. 2016. Early emergence of mcr-1 in Escherichia coli from food-producing animals. The Lancet Infectious Diseases, 16(3): 293. doi: 10.1016/S1473-3099(16)00061-X
    Sun J, Zhang HM, Liu YH, Feng YJ. 2018. Towards understanding MCR-like colistin resistance. Trends in Microbiology, 26(9): 794−808. doi: 10.1016/j.tim.2018.02.006
    Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. Journal of Clinical Microbiology, 33(9): 2233−2239. doi: 10.1128/JCM.33.9.2233-2239.1995
    Trung NV, Matamoros S, Carrique-Mas JJ, Nghia NH, Nhung NT, Chieu TTB, Mai HH, Van Rooijen W, Campbell J, Wagenaar JA, Hardon A, Mai NTN, Hieu TQ, Thwaites G, De Jong MD, Schultsz C, Hoa NT. 2017. Zoonotic transmission of mcr-1 colistin resistance gene from small-scale poultry farms, Vietnam. Emerging Infectious Diseases, 23(3): 529−532. doi: 10.3201/eid2303.161553
    Wang CC, Feng Y, Liu LN, Wei L, Kang M, Zong ZY. 2020. Identification of novel mobile colistin resistance gene mcr-10. Emerging Microbes & Infections, 9(1): 508−516.
    Wang J, Ma ZB, Zeng ZL, Yang XW, Huang Y, Liu JH. 2017a. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zoological Research, 38(2): 55−80. doi: 10.24272/j.issn.2095-8137.2017.003
    Wang Y, Tian GB, Zhang R, Shen YB, Tyrrell JM, Huang X, Zhou HW, Lei L, Li HY, Doi Y, Fang Y, Ren HW, Zhong LL, Shen ZQ, Zeng KJ, Wang SL, Liu JH, Wu CM, Walsh TR, Shen JZ. 2017b. Prevalence, risk factors, outcomes, and molecular epidemiology of mcr-1-positive Enterobacteriaceae in patients and healthy adults from China: an epidemiological and clinical study. The Lancet Infectious Diseases, 17(4): 390−399. doi: 10.1016/S1473-3099(16)30527-8
    Wang Y, Zhang RM, Li JY, Wu ZW, Yin WJ, Schwarz S, Tyrrell JM, Zheng YJ, Wang SL, Shen ZQ, Liu ZH, Liu JY, Lei L, Li M, Zhang QD, Wu CM, Zhang QJ, Wu YN, Walsh TR, Shen JZ. 2017c. Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nature Microbiology, 2: 16260. doi: 10.1038/nmicrobiol.2016.260
    Wu RJ, Yi LX, Yu LF, Wang J, Liu YY, Chen XJ, Lv LC, Yang J, Liu JH. 2018. Fitness advantage of mcr-1-bearing IncI2 and IncX4 plasmids in Vitro. Frontiers in Microbiology, 9: 331. doi: 10.3389/fmicb.2018.00331
    Yang YQ, Li YX, Song T, Yang YX, Jiang W, Zhang AY, Guo XY, Liu BH, Wang YX, Lei CW, Xiang R, Wang HN. 2017. Colistin resistance gene mcr-1 and its variant in Escherichia coli isolates from chickens in China. Antimicrob Agents Chemother, 61(5): e01204-16. doi: 10.1128/AAC.01204-16
    Zhang JL, Chen L, Wang JW, Yassin AK, Butaye P, Kelly P, Gong JS, Guo WN, Li J, Li M, Yang F, Feng ZX, Jiang P, Song CL, Wang YY, You JF, Yang Y, Price S, Qi KZ, Kang Y, Wang CM. 2018. Molecular detection of colistin resistance genes (mcr-1, mcr-2 and mcr-3) in nasal/oropharyngeal and anal/cloacal swabs from pigs and poultry. Scientific Reports, 8(1): 3705. doi: 10.1038/s41598-018-22084-4
    Zhi CP, Lv LC, Yu LF, Doi Y, Liu JH. 2016. Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(3): 292−293. doi: 10.1016/S1473-3099(16)00063-3
  • ZR-2020-131 Supplementary Materials.pdf
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(1)  / Tables(1)

    Article Metrics

    Article views (1588) PDF downloads(165) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint