Horizontal transfer of carbapenemase-encoding plasmids and comparison with hospital epidemiology data

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 8, 2016, Pages 4910-4919

  Hardiman, C A ^a   Weingarten, R A ^a   Conlan, S ^b   Khil, P ^a   Dekker, J P ^a   Mathers, A J ^c   Sheppard, A E ^d   Segre, J A ^b   Frank, K M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBAPENEM; CARBAPENEMASE; CARBAPENEMASE KPC; DORIPENEM; ERTAPENEM; GENOMIC DNA; GENTAMICIN; IMIPENEM; KANAMYCIN; MEROPENEM; RESTRICTION ENDONUCLEASE; TETRACYCLINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA LACTAMASE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM CONJUGATION; COMPUTER MODEL; ESCHERICHIA COLI; HORIZONTAL GENE TRANSFER; IN VITRO STUDY; KLEBSIELLA PNEUMONIAE; NONHUMAN; PLASMID; PRIORITY JOURNAL; CROSS INFECTION; ESCHERICHIA COLI INFECTION; GENETICS; HOSPITAL; HUMAN; KLEBSIELLA INFECTION; MICROBIOLOGY; MULTILOCUS SEQUENCE TYPING; PROCEDURES;

BACTERIAL PROTEINS; BETA-LACTAMASES; CROSS INFECTION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE TRANSFER, HORIZONTAL; HOSPITALS; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MULTILOCUS SEQUENCE TYPING; PLASMIDS;

EID: 84979609071     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00014-16     Document Type: Article

References (56)

1. Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention, Atlanta, GA.
2. Mathers AJ, Cox HL, Kitchel B, Bonatti H, Brassinga AK, Carroll J, Scheld WM, Hazen KC, Sifri CD. 2011. Molecular dissection of an outbreak of carbapenem-resistant Enterobacteriaceae reveals intergenus KPC carbapenemase transmission through a promiscuous plasmid. mBio 2:e00204-11. http://dx.doi.org/10.1128/mBio.00204-11.
3. Perez F, Van Duin D. 2013. Carbapenem-resistant Enterobacteriaceae: a menace to our most vulnerable patients. Cleve Clin J Med 80:225-233. http://dx.doi.org/10.3949/ccjm.80a.12182.
4. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, NISC Comparative Sequencing Program Group, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4:148ra116. http://dx.doi.org/10.1126/scitranslmed.3004129.
5. Viau R, Frank KM, Jacobs MR, Wilson B, Kaye K, Donskey CJ, Perez F, Endimiani A, Bonomo RA. 2016. Intestinal carriage of carbapenemase-producing organisms: current status of surveillance methods. Clin Microbiol Rev 29:1-27. http://dx.doi.org/10.1128/CMR.00108-14.
6. Andrade LN, Curiao T, Ferreira JC, Longo JM, Climaco EC, Martinez R, Bellissimo-Rodrigues F, Basile-Filho A, Evaristo MA, Del Peloso PF, Ribeiro VB, Barth AL, Paula MC, Baquero F, Canton R, Darini AL, Coque TM. 2011. Dissemination of blaKPC-2 by the spread of Klebsiella pneumoniae clonal complex 258 clones (ST258, ST11, ST437) and plasmids (IncFII, IncN, IncL/M) among Enterobacteriaceae species in Brazil. Antimicrob Agents Chemother 55:3579-3583. http://dx.doi.org/10.1128/AAC.01783-10.
7. Chiu SK, Wu TL, Chuang YC, Lin JC, Fung CP, Lu PL, Wang JT, Wang LS, Siu LK, Yeh KM. 2013. National surveillance study on carbapenem non-susceptible Klebsiella pneumoniae in Taiwan: the emergence and rapid dissemination of KPC-2 carbapenemase. PLoS One 8:e69428. http://dx.doi.org/10.1371/journal.pone.0069428.
8. Leavitt A, Chmelnitsky I, Ofek I, Carmeli Y, Navon-Venezia S. 2010. Plasmid pKpQIL encoding KPC-3 and TEM-1 confers carbapenem resistance in an extremely drug-resistant epidemic Klebsiella pneumoniae strain. J Antimicrob Chemother 65:243-248. http://dx.doi.org/10.1093/jac/dkp417.
9. Adler A, Miller-Roll T, Assous MV, Geffen Y, Paikin S, Schwartz D, Weiner-Well Y, Hussein K, Cohen R, Carmeli Y. 2015. A multicenter study of the clonal structure and resistance mechanism of KPC-producing Escherichia coli isolates in Israel. Clin Microbiol Infect 21:230-235. http://dx.doi.org/10.1016/j.cmi.2014.10.008.
10. Kitchel B, Rasheed JK, Patel JB, Srinivasan A, Navon-Venezia S, Carmeli Y, Brolund A, Giske CG. 2009. Molecular epidemiology of KPCproducing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother 53:3365-3370. http://dx.doi.org/10.1128/AAC.00126-09.
11. Deleo FR, Chen L, Porcella SF, Martens CA, Kobayashi SD, Porter AR, Chavda KD, Jacobs MR, Mathema B, Olsen RJ, Bonomo RA, Musser JM, Kreiswirth BN. 2014. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. Proc Natl Acad Sci U S A 111:4988-4993. http://dx.doi.org/10.1073/pnas.1321364111.
12. Patel G, Bonomo RA. 2013. "Stormy waters ahead": global emergence of carbapenemases. Front Microbiol 4:48. http://dx.doi.org/10.3389/fmicb.2013.00048.
13. Woodford N, Turton JF, Livermore DM. 2011. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 35:736-755. http://dx.doi.org/10.1111/j.1574-6976.2011.00268.x.
14. Bowers JR, Kitchel B, Driebe EM, MacCannell DR, Roe C, Lemmer D, de Man T, Rasheed JK, Engelthaler DM, Keim P, Limbago BM. 2015. Genomic analysis of the emergence and rapid global dissemination of the clonal group 258 Klebsiella pneumoniae pandemic. PLoS One 10: e0133727. http://dx.doi.org/10.1371/journal.pone.0133727.
15. Mathers AJ, Peirano G, Pitout JD. 2015. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 28:565-591. http://dx.doi.org/10.1128/CMR.00116-14.
16. Chmelnitsky I, Shklyar M, Hermesh O, Navon-Venezia S, Edgar R, Carmeli Y. 2013. Unique genes identified in the epidemic extremely drug-resistant KPC-producing Klebsiella pneumoniae sequence type 258. J Antimicrob Chemother 68:74-83. http://dx.doi.org/10.1093/jac/dks370.
17. Pitout JD, Nordmann P, Poirel L. 2015. Carbapenemase-producing Klebsiella pneumoniae: a key pathogen set for global nosocomial dominance. Antimicrob Agents Chemother 59:5873-5884. http://dx.doi.org/10.1128/AAC.01019-15.
18. Chen L, Mathema B, Pitout JD, DeLeo FR, Kreiswirth BN. 2014. Epidemic Klebsiella pneumoniae ST258 is a hybrid strain. mBio 5:e01355-14. http://dx.doi.org/10.1128/mBio.01355-14.
19. Thomas CM, Nielsen KM. 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711-721. http://dx.doi.org/10.1038/nrmicro1234.
20. Naas T, Cuzon G, Villegas MV, Lartigue MF, Quinn JP, Nordmann P. 2008. Genetic structures at the origin of acquisition of the beta-lactamase bla KPC gene. Antimicrob Agents Chemother 52:1257-1263. http://dx.doi.org/10.1128/AAC.01451-07.
21. Conlan S, Thomas PJ, Deming C, Park M, Lau AF, Dekker JP, Snitkin ES, Clark TA, Luong K, Song Y, Tsai YC, Boitano M, Dayal J, Brooks SY, Schmidt B, Young AC, Thomas JW, Bouffard GG, Blakesley RW, NISC Comparative Sequencing Program, Mullikin JC, Korlach J, Henderson DK, Frank KM, Palmore TN, Segre JA. 2014. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci Transl Med 6:254ra126. http://dx.doi.org/10.1126/scitranslmed.3009845.
22. Adler A, Khabra E, Paikin S, Carmeli Y. 12 April 2016. Dissemination of the blaKPC gene by clonal spread and horizontal gene transfer: comparative study of incidence and molecular mechanisms. J Antimicrob Chemother. Epub ahead of print.
23. Arnold RS, Thom KA, Sharma S, Phillips M, Kristie Johnson J, Morgan DJ. 2011. Emergence of Klebsiella pneumoniae carbapenemase-producing bacteria. South Med J 104:40-45. http://dx.doi.org/10.1097/SMJ.0b013e3181fd7d5a.
24. Picao RC, Cardoso JP, Campana EH, Nicoletti AG, Petrolini FV, Assis DM, Juliano L, Gales AC. 2013. The route of antimicrobial resistance from the hospital effluent to the environment: focus on the occurrence of KPC-producing Aeromonas spp. and Enterobacteriaceae in sewage. Diagn Microbiol Infect Dis 76:80-85. http://dx.doi.org/10.1016/j.diagmicrobio.2013.02.001.
25. Tavares CP, Pereira PS, Marques Ede A, Faria C, Jr, de Souza Mda P, de Almeida R, Alves Cde F, Asensi MD, Carvalho-Assef AP. 2015. Molecular epidemiology of KPC-2-producing Enterobacteriaceae (non-Klebsiella pneumoniae) isolated from Brazil. Diagn Microbiol Infect Dis 82:326-330. http://dx.doi.org/10.1016/j.diagmicrobio.2015.04.002.
26. Aminov RI. 2011. Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158. http://dx.doi.org/10.3389/fmicb.2011.00158.
27. Goren MG, Carmeli Y, Schwaber MJ, Chmelnitsky I, Schechner V, Navon-Venezia S. 2010. Transfer of carbapenem-resistant plasmid from Klebsiella pneumoniae ST258 to Escherichia coli in patient. Emerg Infect Dis 16:1014-1017. http://dx.doi.org/10.3201/eid1606.091671.
28. Sidjabat HE, Silveira FP, Potoski BA, Abu-Elmagd KM, Adams-Haduch JM, Paterson DL, Doi Y. 2009. Interspecies spread of Klebsiella pneumoniae carbapenemase gene in a single patient. Clin Infect Dis 49:1736-1738. http://dx.doi.org/10.1086/648077.
29. Dortet L, Oueslati S, Jeannot K, Tande D, Naas T, Nordmann P. 2015. Genetic and biochemical characterization of OXA-405, an OXA-48-type extended-spectrum beta-lactamase without significant carbapenemase activity. Antimicrob Agents Chemother 59:3823-3828. http://dx.doi.org/10.1128/AAC.05058-14.
30. Sheppard AE, Stoesser N, Wilson DJ, Sebra R, Kasarskis A, Anson LW, Giess A, Pankhurst LJ, Vaughan A, Grim CJ, Cox HL, Yeh AJ, Modernising Medical Microbiology Informatics Group, Sifri CD, Walker AS, Peto TE, Crook DW, Mathers AJ. 2016. Nested Russian doll-like genetic mobility drives rapid dissemination of the carbapenem resistance gene blaKPC. Antimicrob Agents Chemother 60:3767-3778. http://dx.doi.org/10.1128/AAC.00464-16.
31. Mathers AJ, Stoesser N, Sheppard AE, Pankhurst L, Giess A, Yeh AJ, Didelot X, Turner SD, Sebra R, Kasarskis A, Peto T, Crook D, Sifri CD. 2015. Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae at a single institution: insights into endemicity from wholegenome sequencing. Antimicrob Agents Chemother 59:1656-1663. http://dx.doi.org/10.1128/AAC.04292-14.
32. Lau AF, Wang H, Weingarten RA, Drake SK, Suffredini AF, Garfield MK, Chen Y, Gucek M, Youn JH, Stock F, Tso H, DeLeo J, Cimino JJ, Frank KM, Dekker JP. 2014. A rapid matrix-assisted laser desorption ionization-time of flight mass spectrometry-based method for single-plasmid tracking in an outbreak of carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 52:2804-2812. http://dx.doi.org/10.1128/JCM.00694-14.
33. Leavitt A, Chmelnitsky I, Carmeli Y, Navon-Venezia S. 2010. Complete nucleotide sequence of KPC-3-encoding plasmid pKpQIL in the epidemic Klebsiella pneumoniae sequence type 258. Antimicrob Agents Chemother 54:4493-4496. http://dx.doi.org/10.1128/AAC.00175-10.
34. Sheppard AE, Stoesser N, Sebra R, Kasarskis A, Deikus G, Anson L, Walker AS, Peto TE, Crook DW, Mathers AJ. 2016. Complete genome sequence of KPC-producing Klebsiella pneumoniae strain CAV1193. Genome Announc 4(1):e01649-15. http://dx.doi.org/10.1128/genomeA.01649-15.
35. Wang M, Tran JH, Jacoby GA, Zhang Y, Wang F, Hooper DC. 2003. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob Agents Chemother 47:2242-2248. http://dx.doi.org/10.1128/AAC.47.7.2242-2248.2003.
36. Garcia-Fernandez A, Villa L, Moodley A, Hasman H, Miriagou V, Guardabassi L, Carattoli A. 2011. Multilocus sequence typing of IncN plasmids. J Antimicrob Chemother 66:1987-1991. http://dx.doi.org/10.1093/jac/dkr225.
37. Villa L, Garcia-Fernandez A, Fortini D, Carattoli A. 2010. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 65:2518-2529. http://dx.doi.org/10.1093/jac/dkq347.
38. Novick RP. 1987. Plasmid incompatibility. Microbiol Rev 51:381-395.
39. Hidalgo-Grass C, Warburg G, Temper V, Benenson S, Moses AE, Block C, Strahilevitz J. 2012. KPC-9, a novel carbapenemase from clinical specimens in Israel. Antimicrob Agents Chemother 56:6057-6059. http://dx.doi.org/10.1128/AAC.01156-12.
40. Suzuki H, Yano H, Brown CJ, Top EM. 2010. Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192:6045-6055. http://dx.doi.org/10.1128/JB.00277-10.
41. Chen L, Chavda KD, Melano RG, Hong T, Rojtman AD, Jacobs MR, Bonomo RA, Kreiswirth BN. 2014. Molecular survey of the dissemination of two blaKPC-harboring IncFIA plasmids in New Jersey and New York hospitals. Antimicrob Agents Chemother 58:2289-2294. http://dx.doi.org/10.1128/AAC.02749-13.
42. Bradley DE, Taylor DE, Cohen DR. 1980. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J Bacteriol 143:1466-1470.
43. Potron A, Poirel L, Nordmann P. 2011. Plasmid-mediated transfer of the bla(NDM-1) gene in Gram-negative rods. FEMS Microbiol Lett 324:111-116. http://dx.doi.org/10.1111/j.1574-6968.2011.02392.x.
44. Chen YT, Lin JC, Fung CP, Lu PL, Chuang YC, Wu TL, Siu LK. 2014. KPC-2-encoding plasmids from Escherichia coli and Klebsiella pneumoniae in Taiwan. J Antimicrob Chemother 69:628-631. http://dx.doi.org/10.1093/jac/dkt409.
45. Arutyunov D, Frost LS. 2013. F conjugation: back to the beginning. Plasmid 70:18-32. http://dx.doi.org/10.1016/j.plasmid.2013.03.010.
46. Garcillan-Barcia MP, de la Cruz F. 2008. Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60:1-18. http://dx.doi.org/10.1016/j.plasmid.2008.03.002.
47. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161-168.
48. Siu LK, Lin JC, Gomez E, Eng R, Chiang T. 2012. Virulence and plasmid transferability of KPC Klebsiella pneumoniae at the Veterans Affairs Healthcare System of New Jersey. Microb Drug Resist 18:380-384. http://dx.doi.org/10.1089/mdr.2011.0241.
49. Chavda KD, Chen L, Jacobs MR, Bonomo RA, Kreiswirth BN. 25 April 2016. Molecular diversity and plasmid analysis of KPC-producing Escherichia coli. Antimicrob Agents Chemother. Epub ahead of print.
50. Burton B, Dubnau D. 2010. Membrane-associated DNA transport machines. Cold Spring Harb Perspect Biol 2:a000406. http://dx.doi.org/10.1101/cshperspect.a000406.
51. Freter R, Freter RR, Brickner H. 1983. Experimental and mathematical models of Escherichia coli plasmid transfer in vitro and in vivo. Infect Immun 39:60-84.
52. Gordon DM. 1992. Rate of plasmid transfer among Escherichia coli strains isolated from natural populations. J Gen Microbiol 138:17-21. http://dx.doi.org/10.1099/00221287-138-1-17.
53. Lereclus D, Menou G, Lecadet MM. 1983. Isolation of a DNA sequence related to several plasmids from Bacillus thuringiensis after a mating involving the Streptococcus faecalis plasmid pAM beta 1. Mol Gen Genet 191:307-313. http://dx.doi.org/10.1007/BF00334831.
54. - R factors. Nature 234:222-223. http://dx.doi.org/10.1038/234222a0.
55. Perez-Mendoza D, de la Cruz F. 2009. Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any? BMC Genomics 10:71. http://dx.doi.org/10.1186/1471-2164-10-71.
56. Achtman M, Kennedy N, Skurray R. 1977. Cell-cell interactions in conjugating Escherichia coli: role of traT protein in surface exclusion. Proc Natl Acad Sci U S A 74:5104-5108. http://dx.doi.org/10.1073/pnas.74.11.5104.