Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian Hospital

C. Venditti; D. Fortini; L. Villa; A. Vulcano; S. D’Arezzo; A. Capone; N. Petrosillo; C. Nisii; A. Carattoli; A. Di Caro

doi:10.1128/AAC.00505-17

Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian Hospital

C. Venditti, D. Fortini, L. Villa, A. Vulcano, S. D’Arezzo, A. Capone, N. Petrosillo, C. Nisii, A. Carattoli, A. Di Caro

Research output: Contribution to journal › Article

Abstract

Colonizations due to carbapenem-resistant Enterobacteriaceae (CRE) are a source of antimicrobial resistance transmission in health care settings. Eleven Citrobacter freundii strains producing KPC-3 carbapenemase were isolated from rectal swabs during a 3-year surveillance program. blaKPC-3-carrying plasmids were found to belong to the IncX3 group in 9 of the 11 strains, and complete nucleotide sequences were obtained for 2 of them. Our results highlight the possible role of C. freundii as reservoir of resistance genes. © 2017 American Society for Microbiology. All Rights Reserved.

Original language	English
Journal	Antimicrobial Agents and Chemotherapy
Volume	61
Issue number	8
DOIs	https://doi.org/10.1128/AAC.00505-17
Publication status	Published - 2017

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Keywords

Antibiotic resistance
Citrobacter freundii
IncX3
KPC
KPC-3
bacterial enzyme
beta lactamase
beta lactamase KPC 3
nucleotide
unclassified drug
Article
bacterial strain
bacterium isolation
Italy
nonhuman
nucleotide sequence
plasmid
priority journal

Cite this

Venditti, C., Fortini, D., Villa, L., Vulcano, A., D’Arezzo, S., Capone, A., Petrosillo, N., Nisii, C., Carattoli, A., & Di Caro, A. (2017). Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian Hospital. Antimicrobial Agents and Chemotherapy, 61(8). https://doi.org/10.1128/AAC.00505-17

@article{d143217c1e0b4676a4a670e15494a4f3,

title = "Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian Hospital",

abstract = "Colonizations due to carbapenem-resistant Enterobacteriaceae (CRE) are a source of antimicrobial resistance transmission in health care settings. Eleven Citrobacter freundii strains producing KPC-3 carbapenemase were isolated from rectal swabs during a 3-year surveillance program. blaKPC-3-carrying plasmids were found to belong to the IncX3 group in 9 of the 11 strains, and complete nucleotide sequences were obtained for 2 of them. Our results highlight the possible role of C. freundii as reservoir of resistance genes. {\textcopyright} 2017 American Society for Microbiology. All Rights Reserved.",

keywords = "Antibiotic resistance, Citrobacter freundii, IncX3, KPC, KPC-3, bacterial enzyme, beta lactamase, beta lactamase KPC 3, nucleotide, unclassified drug, Article, bacterial strain, bacterium isolation, Italy, nonhuman, nucleotide sequence, plasmid, priority journal",

author = "C. Venditti and D. Fortini and L. Villa and A. Vulcano and S. D{\textquoteright}Arezzo and A. Capone and N. Petrosillo and C. Nisii and A. Carattoli and {Di Caro}, A.",

note = "Cited By :1 Export Date: 16 April 2018 CODEN: AMACC Correspondence Address: Di Caro, A.; National Institute for Infectious Diseases (INMI) L. SpallanzaniItaly; email: antonino.dicaro@inmi.it Molecular Sequence Numbers: GENBANK: KY659387:KY659388; Chemicals/CAS: beta lactamase, 9073-60-3 References: Giani, T., Pini, B., Arena, F., Conte, V., Bracco, S., Migliavacca, R., Pantosti, A., Rossolini, G.M., Epidemic diffusion of KPC carbapenemase-producing Klebsiella pneumoniae in Italy: Results of the first countrywide survey, 15 May to 30 June 2011 (2013) Euro Surveill, 30 (22), p. 18. , http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId20489; Munoz-Price, L.S., Poirel, L., Bonomo, R.A., Schwaber, M.J., Daikos, G.L., Cormican, M., Cornaglia, G., Quinn, J.P., Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases (2013) Lancet Infect Dis, 13, pp. 785-796. , https://doi.org/10.1016/S1473-3099(13)70190-7; Naas, T., Cuzon, G., Villegas, M.V., Lartigue, M.F., Quinn, J.P., Nordmann, P., Genetic structures at the origin of acquisition of the beta-lactamase blaKPC gene (2008) Antimicrob Agents Chemother, 52, pp. 1257-1263. , https://doi.org/10.1128/AAC.01451-07; Zhang, R., Yang, L., Cai, J.C., Zhou, H.W., Chen, G.X., High-level carbapenem resistance in a Citrobacter freundii clinical isolate is due to a combination of KPC-2 production and decreased porin expression (2008) J Med Microbiol, 57, pp. 332-337. , https://doi.org/10.1099/jmm.0.47576-0; Adler, A., Khabra, E., Paikin, S., Carmeli, Y., Dissemination of the blaKPC gene by clonal spread and horizontal gene transfer: Comparative study of incidence and molecular mechanisms (2016) J Antimicrob Chemother, 71, pp. 2143-2146. , https://doi.org/10.1093/jac/dkw106; Ribeiro, T.G., Novais, {\^A}., Branquinho, R., Machado, E., Peixe, L., Phylogeny and comparative genomics unveil independent diversification trajectories of qnrB and genetic platforms within particular Citrobacter species (2015) Antimicrob Agents Chemother, 59, pp. 5951-5958. , https://doi.org/10.1128/AAC.00027-15; Ribeiro, T.G., Clermont, D., Branquinho, R., Machado, E., Peixe, L., Brisse, S., Citrobacter europaeus sp. Nov., isolated from water and human faecal samples (2017) Int J Syst Evol Microbiol, 67, pp. 170-173. , https://doi.org/10.1099/ijsem.0.001606; (2015) M07-A10. Methods for Dilution Antimicrobial Susceptibility Test for Bacteria That Grow Aerobically; Approved Standard, , Clinical and Laboratory Standards Institute (CLSI). 10th ed. CLSI, Wayne, PA; Bai, L., Xia, S., Lan, R., Liu, L., Ye, C., Wang, Y., Jin, D., Xu, J., Isolation and characterization of cytotoxic, aggregative Citrobacter freundii (2012) Plos One, 7. , https://doi.org/10.1371/journal.pone.0033054; Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L.H., Karch, H., Achtman, M., Sex and virulence in Escherichia coli: An evolutionary perspective (2006) Mol Microbiol, 60, pp. 1136-1151. , https://doi.org/10.1111/j.1365-2958.2006.05172.x; Lunha, K., Chanawong, A., Lulitanond, A., Wilailuckana, C., Charoensri, N., Wonglakorn, L., Saenjamla, P., Chetchotisakd, P., High-level carbapenem-resistant OXA-48-producing Klebsiella pneumoniae with a novel OmpK36 variant and low-level, carbapenem-resistant, non-porin-deficient, OXA-181-producing Escherichia coli from Thailand (2016) Diagn Microbiol Infect Dis, 85, pp. 221-226. , https://doi.org/10.1016/j.diagmicrobio.2016.03.009; Dortet, L., Poirel, L., Anguel, N., Nordmann, P., New Delhi metallo-β-lactamase 4-producing Escherichia coli in Cameroon (2012) Emerg Infect Dis, 18, pp. 1540-1542. , https://doi.org/10.3201/eid1809.120011; Peirano, G., Lascols, C., Hackel, M., Hoban, D.J., Pitout, J.D., Molecular epidemiology of Enterobacteriaceae that produce VIMs and IMPs from the SMART surveillance program (2014) Diagn Microbiol Infect Dis, 78, pp. 277-281. , https://doi.org/10.1016/j.diagmicrobio.2013.11.024; Poirel, L., Walsh, T.R., Cuvillier, V., Nordmann, P., Multiplex PCR for detection of acquired carbapenemase genes (2011) Diagn Microbiol Infect Dis, 70, pp. S119-S123. , https://doi.org/10.1016/j.diagmicrobio.2010.12.002; Mabilat, C., Goussard, S., Sougakoff, W., Spencer, R.C., Courvalin, P., Direct sequencing of the amplified structural gene and promoter for the extended-broad-spectrum beta-lactamase TEM-9 (RHH-1) of Klebsiella pneumoniae (1990) Plasmid, 23, pp. S27-S34. , https://doi.org/10.1016/0147-619X(90)90041-A; Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K.L., Threlfall, E.J., Identification of plasmids by PCR-based replicon typing (2005) J Microbiol Methods, 63, pp. S219-S228. , https://doi.org/10.1016/j.mimet.2005.03.018; Tritt, A., Eisen, J.A., Facciotti, M.T., Darling, A.E., An integrated pipeline for de novo assembly of microbial genomes (2012) Plos One, 7. , https://doi.org/10.1371/journal.pone.0042304; Garc{\'i}a-Fern{\'a}ndez, A., Villa, L., Carta, C., Venditti, C., Giordano, A., Venditti, M., Mancini, C., Carattoli, A., Klebsiella pneumoniae ST258 producing KPC-3 identified in Italy carries novel plasmids and OmpK36/OmpK35 porin variants (2012) Antimicrob Agents Chemother, 56, pp. 2143-2145. , https://doi.org/10.1128/AAC.05308-11; Ho, P.L., Cheung, Y.Y., Lo, W.U., Li, Z., Chow, K.H., Lin, C.H., Chan, J.F., Cheng, V.C., Molecular characterization of an atypical IncX3 plasmid pKPC-NY79 carrying blaKPC-2 in a Klebsiella pneumoniae (2013) Curr Microbiol, 67, pp. 493-498. , https://doi.org/10.1007/s00284-013-0398-2; Ho, P.L., Li, Z., Lo, W.U., Cheung, Y.Y., Lin, C.H., Sham, P.C., Cheng, V.C., Chow, K.H., Identification and characterization of a novel incompatibility group X3 plasmid carrying blaNDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China (2012) Emerg Microbes Infect, 1, p. e39. , https://doi.org/10.1038/emi.2012.37; Feng, J., Qiu, Y., Yin, Z., Chen, W., Yang, H., Yang, W., Wang, J., Zhou, D., Coexistence of a novel KPC-2-encoding MDR plasmid and an NDM-1-encoding pNDM-HN380-like plasmid in a clinical isolate of Citrobacter freundii (2015) J Antimicrob Chemother, 70, pp. 2987-2991. , https://doi.org/10.1093/jac/dkv232",

year = "2017",

doi = "10.1128/AAC.00505-17",

language = "English",

volume = "61",

journal = "Antimicrobial Agents and Chemotherapy",

issn = "0066-4804",

publisher = "American Society for Microbiology",

number = "8",

}

TY - JOUR

T1 - Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian Hospital

AU - Venditti, C.

AU - Fortini, D.

AU - Villa, L.

AU - Vulcano, A.

AU - D’Arezzo, S.

AU - Capone, A.

AU - Petrosillo, N.

AU - Nisii, C.

AU - Carattoli, A.

AU - Di Caro, A.

N1 - Cited By :1 Export Date: 16 April 2018 CODEN: AMACC Correspondence Address: Di Caro, A.; National Institute for Infectious Diseases (INMI) L. SpallanzaniItaly; email: antonino.dicaro@inmi.it Molecular Sequence Numbers: GENBANK: KY659387:KY659388; Chemicals/CAS: beta lactamase, 9073-60-3 References: Giani, T., Pini, B., Arena, F., Conte, V., Bracco, S., Migliavacca, R., Pantosti, A., Rossolini, G.M., Epidemic diffusion of KPC carbapenemase-producing Klebsiella pneumoniae in Italy: Results of the first countrywide survey, 15 May to 30 June 2011 (2013) Euro Surveill, 30 (22), p. 18. , http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId20489; Munoz-Price, L.S., Poirel, L., Bonomo, R.A., Schwaber, M.J., Daikos, G.L., Cormican, M., Cornaglia, G., Quinn, J.P., Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases (2013) Lancet Infect Dis, 13, pp. 785-796. , https://doi.org/10.1016/S1473-3099(13)70190-7; Naas, T., Cuzon, G., Villegas, M.V., Lartigue, M.F., Quinn, J.P., Nordmann, P., Genetic structures at the origin of acquisition of the beta-lactamase blaKPC gene (2008) Antimicrob Agents Chemother, 52, pp. 1257-1263. , https://doi.org/10.1128/AAC.01451-07; Zhang, R., Yang, L., Cai, J.C., Zhou, H.W., Chen, G.X., High-level carbapenem resistance in a Citrobacter freundii clinical isolate is due to a combination of KPC-2 production and decreased porin expression (2008) J Med Microbiol, 57, pp. 332-337. , https://doi.org/10.1099/jmm.0.47576-0; Adler, A., Khabra, E., Paikin, S., Carmeli, Y., Dissemination of the blaKPC gene by clonal spread and horizontal gene transfer: Comparative study of incidence and molecular mechanisms (2016) J Antimicrob Chemother, 71, pp. 2143-2146. , https://doi.org/10.1093/jac/dkw106; Ribeiro, T.G., Novais, Â., Branquinho, R., Machado, E., Peixe, L., Phylogeny and comparative genomics unveil independent diversification trajectories of qnrB and genetic platforms within particular Citrobacter species (2015) Antimicrob Agents Chemother, 59, pp. 5951-5958. , https://doi.org/10.1128/AAC.00027-15; Ribeiro, T.G., Clermont, D., Branquinho, R., Machado, E., Peixe, L., Brisse, S., Citrobacter europaeus sp. Nov., isolated from water and human faecal samples (2017) Int J Syst Evol Microbiol, 67, pp. 170-173. , https://doi.org/10.1099/ijsem.0.001606; (2015) M07-A10. Methods for Dilution Antimicrobial Susceptibility Test for Bacteria That Grow Aerobically; Approved Standard, , Clinical and Laboratory Standards Institute (CLSI). 10th ed. CLSI, Wayne, PA; Bai, L., Xia, S., Lan, R., Liu, L., Ye, C., Wang, Y., Jin, D., Xu, J., Isolation and characterization of cytotoxic, aggregative Citrobacter freundii (2012) Plos One, 7. , https://doi.org/10.1371/journal.pone.0033054; Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L.H., Karch, H., Achtman, M., Sex and virulence in Escherichia coli: An evolutionary perspective (2006) Mol Microbiol, 60, pp. 1136-1151. , https://doi.org/10.1111/j.1365-2958.2006.05172.x; Lunha, K., Chanawong, A., Lulitanond, A., Wilailuckana, C., Charoensri, N., Wonglakorn, L., Saenjamla, P., Chetchotisakd, P., High-level carbapenem-resistant OXA-48-producing Klebsiella pneumoniae with a novel OmpK36 variant and low-level, carbapenem-resistant, non-porin-deficient, OXA-181-producing Escherichia coli from Thailand (2016) Diagn Microbiol Infect Dis, 85, pp. 221-226. , https://doi.org/10.1016/j.diagmicrobio.2016.03.009; Dortet, L., Poirel, L., Anguel, N., Nordmann, P., New Delhi metallo-β-lactamase 4-producing Escherichia coli in Cameroon (2012) Emerg Infect Dis, 18, pp. 1540-1542. , https://doi.org/10.3201/eid1809.120011; Peirano, G., Lascols, C., Hackel, M., Hoban, D.J., Pitout, J.D., Molecular epidemiology of Enterobacteriaceae that produce VIMs and IMPs from the SMART surveillance program (2014) Diagn Microbiol Infect Dis, 78, pp. 277-281. , https://doi.org/10.1016/j.diagmicrobio.2013.11.024; Poirel, L., Walsh, T.R., Cuvillier, V., Nordmann, P., Multiplex PCR for detection of acquired carbapenemase genes (2011) Diagn Microbiol Infect Dis, 70, pp. S119-S123. , https://doi.org/10.1016/j.diagmicrobio.2010.12.002; Mabilat, C., Goussard, S., Sougakoff, W., Spencer, R.C., Courvalin, P., Direct sequencing of the amplified structural gene and promoter for the extended-broad-spectrum beta-lactamase TEM-9 (RHH-1) of Klebsiella pneumoniae (1990) Plasmid, 23, pp. S27-S34. , https://doi.org/10.1016/0147-619X(90)90041-A; Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K.L., Threlfall, E.J., Identification of plasmids by PCR-based replicon typing (2005) J Microbiol Methods, 63, pp. S219-S228. , https://doi.org/10.1016/j.mimet.2005.03.018; Tritt, A., Eisen, J.A., Facciotti, M.T., Darling, A.E., An integrated pipeline for de novo assembly of microbial genomes (2012) Plos One, 7. , https://doi.org/10.1371/journal.pone.0042304; García-Fernández, A., Villa, L., Carta, C., Venditti, C., Giordano, A., Venditti, M., Mancini, C., Carattoli, A., Klebsiella pneumoniae ST258 producing KPC-3 identified in Italy carries novel plasmids and OmpK36/OmpK35 porin variants (2012) Antimicrob Agents Chemother, 56, pp. 2143-2145. , https://doi.org/10.1128/AAC.05308-11; Ho, P.L., Cheung, Y.Y., Lo, W.U., Li, Z., Chow, K.H., Lin, C.H., Chan, J.F., Cheng, V.C., Molecular characterization of an atypical IncX3 plasmid pKPC-NY79 carrying blaKPC-2 in a Klebsiella pneumoniae (2013) Curr Microbiol, 67, pp. 493-498. , https://doi.org/10.1007/s00284-013-0398-2; Ho, P.L., Li, Z., Lo, W.U., Cheung, Y.Y., Lin, C.H., Sham, P.C., Cheng, V.C., Chow, K.H., Identification and characterization of a novel incompatibility group X3 plasmid carrying blaNDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China (2012) Emerg Microbes Infect, 1, p. e39. , https://doi.org/10.1038/emi.2012.37; Feng, J., Qiu, Y., Yin, Z., Chen, W., Yang, H., Yang, W., Wang, J., Zhou, D., Coexistence of a novel KPC-2-encoding MDR plasmid and an NDM-1-encoding pNDM-HN380-like plasmid in a clinical isolate of Citrobacter freundii (2015) J Antimicrob Chemother, 70, pp. 2987-2991. , https://doi.org/10.1093/jac/dkv232

PY - 2017

Y1 - 2017

N2 - Colonizations due to carbapenem-resistant Enterobacteriaceae (CRE) are a source of antimicrobial resistance transmission in health care settings. Eleven Citrobacter freundii strains producing KPC-3 carbapenemase were isolated from rectal swabs during a 3-year surveillance program. blaKPC-3-carrying plasmids were found to belong to the IncX3 group in 9 of the 11 strains, and complete nucleotide sequences were obtained for 2 of them. Our results highlight the possible role of C. freundii as reservoir of resistance genes. © 2017 American Society for Microbiology. All Rights Reserved.

AB - Colonizations due to carbapenem-resistant Enterobacteriaceae (CRE) are a source of antimicrobial resistance transmission in health care settings. Eleven Citrobacter freundii strains producing KPC-3 carbapenemase were isolated from rectal swabs during a 3-year surveillance program. blaKPC-3-carrying plasmids were found to belong to the IncX3 group in 9 of the 11 strains, and complete nucleotide sequences were obtained for 2 of them. Our results highlight the possible role of C. freundii as reservoir of resistance genes. © 2017 American Society for Microbiology. All Rights Reserved.

KW - Antibiotic resistance

KW - Citrobacter freundii

KW - IncX3

KW - KPC

KW - KPC-3

KW - bacterial enzyme

KW - beta lactamase

KW - beta lactamase KPC 3

KW - nucleotide

KW - unclassified drug

KW - Article

KW - bacterial strain

KW - bacterium isolation

KW - Italy

KW - nonhuman

KW - nucleotide sequence

KW - plasmid

KW - priority journal

U2 - 10.1128/AAC.00505-17

DO - 10.1128/AAC.00505-17

M3 - Article

VL - 61

JO - Antimicrobial Agents and Chemotherapy

JF - Antimicrobial Agents and Chemotherapy

SN - 0066-4804

IS - 8

ER -

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