Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
BMC Infectious Diseases
Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | Research article

Genomic surveillance for multidrug-resistant or hypervirulent Klebsiella pneumoniae among United States bloodstream isolates

Authors: Travis J. Kochan, Sophia H. Nozick, Rachel L. Medernach, Bettina H. Cheung, Samuel W. M. Gatesy, Marine Lebrun-Corbin, Sumitra D. Mitra, Natalia Khalatyan, Fiorella Krapp, Chao Qi, Egon A. Ozer, Alan R. Hauser

Published in: BMC Infectious Diseases | Issue 1/2022

Login to get access

Abstract

Background

Klebsiella pneumoniae strains have been divided into two major categories: classical K. pneumoniae, which are frequently multidrug-resistant and cause hospital-acquired infections in patients with impaired defenses, and hypervirulent K. pneumoniae, which cause severe community-acquired and disseminated infections in normal hosts. Both types of infections may lead to bacteremia and are associated with significant morbidity and mortality. The relative burden of these two types of K. pneumoniae among bloodstream isolates within the United States is not well understood.

Methods

We evaluated consecutive K. pneumoniae isolates cultured from the blood of hospitalized patients at Northwestern Memorial Hospital (NMH) in Chicago, Illinois between April 2015 and April 2017. Bloodstream isolates underwent whole genome sequencing, and sequence types (STs), capsule loci (KLs), virulence genes, and antimicrobial resistance genes were identified in the genomes using the bioinformatic tools Kleborate and Kaptive. Patient demographic, comorbidity, and infection information, as well as the phenotypic antimicrobial resistance of the isolates were extracted from the electronic health record. Candidate hypervirulent isolates were tested in a murine model of pneumonia, and their plasmids were characterized using long-read sequencing. We also extracted STs, KLs, and virulence and antimicrobial resistance genes from the genomes of bloodstream isolates submitted from 33 United States institutions between 2007 and 2021 to the National Center for Biotechnology Information (NCBI) database.

Results

Consecutive K. pneumoniae bloodstream isolates (n = 104, one per patient) from NMH consisted of 75 distinct STs and 51 unique capsule loci. The majority of these isolates (n = 58, 55.8%) were susceptible to all tested antibiotics except ampicillin, but 17 (16.3%) were multidrug-resistant. A total of 32 (30.8%) of these isolates were STs of known high-risk clones, including ST258 and ST45. In particular, 18 (17.3%) were resistant to ceftriaxone (of which 17 harbored extended-spectrum beta-lactamase genes) and 9 (8.7%) were resistant to meropenem (all of which harbored a carbapenemase genes). Four (3.8%) of the 104 isolates were hypervirulent K. pneumoniae, as evidenced by hypermucoviscous phenotypes, high levels of virulence in a murine model of pneumonia, and the presence of large plasmids similar to characterized hypervirulence plasmids. These isolates were cultured from patients who had not recently traveled to Asia. Two of these hypervirulent isolates belonged to the well characterized ST23 lineage and one to the re-emerging ST66 lineage. Of particular concern, two of these isolates contained plasmids with tra conjugation loci suggesting the potential for transmission. We also analyzed 963 publicly available genomes of K. pneumoniae bloodstream isolates from locations within the United States. Of these, 465 (48.3%) and 760 (78.9%) contained extended-spectrum beta-lactamase genes or carbapenemase genes, respectively, suggesting a bias towards submission of antibiotic-resistant isolates. The known multidrug-resistant high-risk clones ST258 and ST307 were the predominant sequence types. A total of 32 (3.3%) of these isolates contained aerobactin biosynthesis genes and 26 (2.7%) contained at least two genetic features of hvKP strains, suggesting elevated levels of virulence. We identified 6 (0.6%) isolates that were STs associated with hvKP: ST23 (n = 4), ST380 (n = 1), and ST65 (n = 1).

Conclusions

Examination of consecutive isolates from a single center demonstrated that multidrug-resistant high-risk clones are indeed common, but a small number of hypervirulent K. pneumoniae isolates were also observed in patients with no recent travel history to Asia, suggesting that these isolates are undergoing community spread in the United States. A larger collection of publicly available bloodstream isolate genomes also suggested that hypervirulent K. pneumoniae strains are present but rare in the USA; however, this collection appears to be heavily biased towards highly antibiotic-resistant isolates (and correspondingly away from hypervirulent isolates).
Appendix
Available only for authorised users
Literature
1.
Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev. 1998;11:589–603.PubMedPubMedCentralCrossRef
2.
Dhesi Z, Enne VI, Brealey D, Livermore DM, High J, Russell C, Colles A, Kandil H, Mack D, Martin D, Page V, Parker R, Roulston K, Singh S, Wey E, Swart AM, Stirling S, Barber JA, O’Grady J, Gant VA. Organisms causing secondary pneumonias in COVID-19 patients at 5 UK ICUs as detected with the FilmArray test. medRvix. 2020. https://​doi.​org/​10.​1101/​2020.​06.​22.​20131573.CrossRef
3.
Li J, Ren J, Wang W, Wang G, Gu G, Wu X, Wang Y, Huang M, Li J. Risk factors and clinical outcomes of hypervirulent Klebsiella pneumoniae induced bloodstream infections. Eur J Clin Microbiol Infect Dis. 2018;37:679–89.PubMedCrossRef
4.
Meatherall BL, Gregson D, Ross T, Pitout JD, Laupland KB. Incidence, risk factors, and outcomes of Klebsiella pneumoniae bacteremia. Am J Med. 2009;122:866–73.PubMedCrossRef
5.
Girometti N, Lewis RE, Giannella M, Ambretti S, Bartoletti M, Tedeschi S, Tumietto F, Cristini F, Trapani F, Gaibani P, Viale P. Klebsiella pneumoniae bloodstream infection: epidemiology and impact of inappropriate empirical therapy. Medicine (Baltimore). 2014;93:298–309.CrossRef
6.
Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev. 2019;32.
7.
Marcade G, Brisse S, Bialek S, Marcon E, Leflon-Guibout V, Passet V, Moreau R, Nicolas-Chanoine MH. The emergence of multidrug-resistant Klebsiella pneumoniae of international clones ST13, ST16, ST35, ST48 and ST101 in a teaching hospital in the Paris region. Epidemiol Infect. 2013;141:1705–12.PubMedCrossRef
8.
Meng X, Yang J, Duan J, Liu S, Huang X, Wen X, Huang X, Fu C, Li J, Dou Q, Liu Y, Wang J, Yan Q, Zou M, Liu W, Peng Z, Chen L, Li C, Wu A. Assessing molecular epidemiology of carbapenem-resistant Klebsiella pneumoniae (CR-KP) with MLST and MALDI-TOF in Central China. Sci Rep. 2019;9:2271.PubMedPubMedCentralCrossRef
9.
Roulston KJ, Bharucha T, Turton JF, Hopkins KL, Mack DJF. A case of NDM-carbapenemase-producing hypervirulent Klebsiella pneumoniae sequence type 23 from the UK. JMM Case Rep. 2018;5: e005130.PubMedPubMedCentralCrossRef
10.
Shen D, Ma G, Li C, Jia X, Qin C, Yang T, Wang L, Jiang X, Ding N, Zhang X, Yue L, Yin Z, Zeng L, Zhao Y, Zhou D, Chen F. Emergence of a multidrug-resistant hypervirulent Klebsiella pneumoniae sequence type 23 strain with a rare bla CTX-M-24-harboring virulence plasmid. Antimicrob Agents Chemother. 2019;63.
11.
Shu L, Dong N, Lu J, Zheng Z, Hu J, Zeng W, Sun Q, Chan EW, Zhou H, Hu F, Chen S, Zhang R. Emergence of OXA-232 carbapenemase-producing Klebsiella pneumoniae that carries a pLVPK-like virulence plasmid among elderly patients in China. Antimicrob Agents Chemother. 2019;63.
12.
Lester CH, Olsen SS, Jakobsen L, Arpi M, Fuursted K, Hansen DS, Heltberg O, Holm A, Hojbjerg T, Jensen KT, Johansen HK, Justesen US, Kemp M, Knudsen JD, Roder B, Frimodt-Moller N, Hammerum AM. Emergence of extended-spectrum beta-lactamase (ESBL)-producing Klebsiella pneumoniae in Danish hospitals; this is in part explained by spread of two CTX-M-15 clones with multilocus sequence types 15 and 16 in Zealand. Int J Antimicrob Agents. 2011;38:180–2.PubMedCrossRef
13.
Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev. 2017;41:252–75.PubMedCrossRef
14.
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. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81.PubMedCrossRef
15.
Turton J, Davies F, Turton J, Perry C, Payne Z, Pike R. Hybrid Resistance and Virulence Plasmids in "High-Risk" Clones of Klebsiella pneumoniae, Including Those Carrying blaNDM-5. Microorganisms. 2019; 7.
16.
Goncalves GB, Furlan JPR, Vespero EC, Pelisson M, Stehling EG, Pitondo-Silva A. Spread of multidrug-resistant high-risk Klebsiella pneumoniae clones in a tertiary hospital from southern Brazil. Infect Genet Evol. 2017;56:1–7.PubMedCrossRef
17.
Nascimento T, Cantamessa R, Melo L, Fernandes MR, Fraga E, Dropa M, Sato MIZ, Cerdeira L, Lincopan N. International high-risk clones of Klebsiella pneumoniae KPC-2/CC258 and Escherichia coli CTX-M-15/CC10 in urban lake waters. Sci Total Environ. 2017;598:910–5.PubMedCrossRef
18.
Oteo J, Perez-Vazquez M, Bautista V, Ortega A, Zamarron P, Saez D, Fernandez-Romero S, Lara N, Ramiro R, Aracil B, Campos J, Spanish Antibiotic Resistance Surveillance Program Collaborating G. The spread of KPC-producing Enterobacteriaceae in Spain: WGS analysis of the emerging high-risk clones of Klebsiella pneumoniae ST11/KPC-2, ST101/KPC-2 and ST512/KPC-3. J Antimicrob Chemother. 2016;71:3392–9.PubMedPubMedCentralCrossRef
19.
Rodriguez I, Novais A, Lira F, Valverde A, Curiao T, Martinez JL, Baquero F, Canton R, Coque TM. Antibiotic-resistant Klebsiella pneumoniae and Escherichia coli high-risk clones and an IncFII(k) mosaic plasmid hosting Tn1 (blaTEM-4) in isolates from 1990 to 2004. Antimicrob Agents Chemother. 2015;59:2904–8.PubMedPubMedCentralCrossRef
20.
Oliveira S, Moura RA, Silva KC, Pavez M, McCulloch JA, Dropa M, Matte MH, Mamizuka EM, Sato MI, Pestana de Castro AF, Lincopan N. Isolation of KPC-2-producing Klebsiella pneumoniae strains belonging to the high-risk multiresistant clonal complex 11 (ST437 and ST340) in urban rivers. J Antimicrob Chemother. 2014;69:849–52.PubMedCrossRef
21.
Wyres KL, Lam MMC, Holt KE. Population genomics of Klebsiella pneumoniae. Nat Rev Microbiol. 2020;18:344–59.PubMedCrossRef
22.
Chmelnitsky I, Doniger T, Shklyar M, Naparstek L, Banin E, Edgar R, Carmeli Y. Draft genome sequence of an extremely drug-resistant KPC-producing Klebsiella pneumoniae ST258 epidemic strain. J Bacteriol. 2012;194:6014.PubMedPubMedCentralCrossRef
23.
Chen L, Chavda KD, Mediavilla JR, Zhao Y, Fraimow HS, Jenkins SG, Levi MH, Hong T, Rojtman AD, Ginocchio CC, Bonomo RA, Kreiswirth BN. Multiplex real-time PCR for detection of an epidemic KPC-producing Klebsiella pneumoniae ST258 clone. Antimicrob Agents Chemother. 2012;56:3444–7.PubMedPubMedCentralCrossRef
24.
Bogdanovich T, Adams-Haduch JM, Tian GB, Nguyen MH, Kwak EJ, Muto CA, Doi Y. Colistin-resistant, Klebsiella pneumoniae carbapenemase (KPC)-producing Klebsiella pneumoniae belonging to the international epidemic clone ST258. Clin Infect Dis. 2011;53:373–6.PubMedPubMedCentralCrossRef
25.
Long SW, Olsen RJ, Eagar TN, Beres SB, Zhao P, Davis JJ, Brettin T, Xia F, Musser JM. Population Genomic Analysis of 1,777 Extended-Spectrum Beta-Lactamase-Producing Klebsiella pneumoniae Isolates, Houston, Texas: Unexpected Abundance of Clonal Group 307. mBio 2017;8.
26.
27.
Talbot GH, Bradley J, Edwards JE Jr, Gilbert D, Scheld M, Bartlett JG. Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin Infect Dis. 2006;42:657–68.PubMedCrossRef
28.
29.
Liu YC, Cheng DL, Lin CL. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med. 1986;146:1913–6.PubMedCrossRef
30.
31.
Lam MMC, Wyres KL, Duchene S, Wick RR, Judd LM, Gan YH, Hoh CH, Archuleta S, Molton JS, Kalimuddin S, Koh TH, Passet V, Brisse S, Holt KE. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat Commun. 2018;9:2703.PubMedPubMedCentralCrossRef
32.
Turton JF, Englender H, Gabriel SN, Turton SE, Kaufmann ME, Pitt TL. Genetically similar isolates of Klebsiella pneumoniae serotype K1 causing liver abscesses in three continents. J Med Microbiol. 2007;56:593–7.PubMedCrossRef
33.
Siu LK, Fung CP, Chang FY, Lee N, Yeh KM, Koh TH, Ip M. Molecular typing and virulence analysis of serotype K1 Klebsiella pneumoniae strains isolated from liver abscess patients and stool samples from noninfectious subjects in Hong Kong, Singapore, and Taiwan. J Clin Microbiol. 2011;49:3761–5.PubMedPubMedCentralCrossRef
34.
Vila A, Cassata A, Pagella H, Amadio C, Yeh KM, Chang FY, Siu LK. Appearance of Klebsiella pneumoniae liver abscess syndrome in Argentina: case report and review of molecular mechanisms of pathogenesis. Open Microbiol J. 2011;5:107–13.PubMedPubMedCentralCrossRef
35.
Pastagia M, Arumugam V. Klebsiella pneumoniae liver abscesses in a public hospital in Queens, New York. Travel Med Infect Dis. 2008;6:228–33.PubMedCrossRef
36.
Rahimian J, Wilson T, Oram V, Holzman RS. Pyogenic liver abscess: recent trends in etiology and mortality. Clin Infect Dis. 2004;39:1654–9.PubMedCrossRef
37.
38.
Peirano G, Pitout JD, Laupland KB, Meatherall B, Gregson DB. Population-based surveillance for hypermucoviscosity Klebsiella pneumoniae causing community-acquired bacteremia in Calgary, Alberta. Can J Infect Dis Med Microbiol. 2013;24:e61–4.PubMedPubMedCentralCrossRef
39.
Chou A, Nuila RE, Franco LM, Stager CE, Atmar RL, Zechiedrich L. Prevalence of hypervirulent Klebsiella pneumoniae-associated genes rmpA and magA in two tertiary hospitals in Houston, TX, USA. J Med Microbiol. 2016;65:1047–8.PubMedPubMedCentralCrossRef
40.
Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U, Hutson A, Barker JH, La Hoz RM, Johnson JR. Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from Classical K. pneumoniae. J Clin Microbiol. 2018;56.
41.
Chen YT, Chang HY, Lai YC, Pan CC, Tsai SF, Peng HL. Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. Gene. 2004;337:189–98.PubMedCrossRef
42.
Nassif X, Fournier JM, Arondel J, Sansonetti PJ. Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect Immun. 1989;57:546–52.PubMedPubMedCentralCrossRef
43.
Wu KM, Li LH, Yan JJ, Tsao N, Liao TL, Tsai HC, Fung CP, Chen HJ, Liu YM, Wang JT, Fang CT, Chang SC, Shu HY, Liu TT, Chen YT, Shiau YR, Lauderdale TL, Su IJ, Kirby R, Tsai SF. Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol. 2009;191:4492–501.PubMedPubMedCentralCrossRef
44.
Lam MMC, Wyres KL, Judd LM, Wick RR, Jenney A, Brisse S, Holt KE. Tracking key virulence loci encoding aerobactin and salmochelin siderophore synthesis in Klebsiella pneumoniae. Genome Med. 2018;10:77.PubMedPubMedCentralCrossRef
45.
Wyres KL, Wick RR, Judd LM, Froumine R, Tokolyi A, Gorrie CL, Lam MMC, Duchene S, Jenney A, Holt KE. Distinct evolutionary dynamics of horizontal gene transfer in drug resistant and virulent clones of Klebsiella pneumoniae. PLoS Genet. 2019;15: e1008114.PubMedPubMedCentralCrossRef
46.
47.
Vornhagen J, Bassis CM, Ramakrishnan S, Hein R, Mason S, Bergman Y, Sunshine N, Fan Y, Holmes CL, Timp W, Schatz MC, Young VB, Simner PJ, Bachman MA. A plasmid locus associated with Klebsiella clinical infections encodes a microbiome-dependent gut fitness factor. PLoS Pathog. 2021;17:e1009537.PubMedPubMedCentralCrossRef
48.
Lery LM, Frangeul L, Tomas A, Passet V, Almeida AS, Bialek-Davenet S, Barbe V, Bengoechea JA, Sansonetti P, Brisse S, Tournebize R. Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor. BMC Biol. 2014;12:41.PubMedPubMedCentralCrossRef
49.
Kochan TJ, Ozer EA, Pincus NB, Fitzpatrick MA, Hauser AR. Complete Genome Sequence of Klebsiella pneumoniae Strain TK421, a Conjugative Hypervirulent Isolate. Microbiol Resour Announc. 2020;9.
50.
Hsieh PF, Lin TL, Lee CZ, Tsai SF, Wang JT. Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis. 2008;197:1717–27.PubMedCrossRef
51.
Russo TA, Olson R, MacDonald U, Beanan J, Davidson BA. Aerobactin, but not yersiniabactin, salmochelin, or enterobactin, enables the growth/survival of hypervirulent (hypermucoviscous) Klebsiella pneumoniae ex vivo and in vivo. Infect Immun. 2015;83:3325–33.PubMedPubMedCentralCrossRef
52.
Lawlor MS, Hsu J, Rick PD, Miller VL. Identification of Klebsiella pneumoniae virulence determinants using an intranasal infection model. Mol Microbiol. 2005;58:1054–73.PubMedCrossRef
53.
Xiong H, Carter RA, Leiner IM, Tang YW, Chen L, Kreiswirth BN, Pamer EG. Distinct contributions of neutrophils and CCR2+ monocytes to pulmonary clearance of different Klebsiella pneumoniae strains. Infect Immun. 2015;83:3418–27.PubMedPubMedCentralCrossRef
54.
Lam MMC, Wick RR, Wyres KL, Gorrie CL, Judd LM, Jenney AWJ, Brisse S, Holt KE. Genetic diversity, mobilisation and spread of the yersiniabactin-encoding mobile element ICEKp in Klebsiella pneumoniae populations. Microb Genom. 2018;4.
55.
Bachman MA, Oyler JE, Burns SH, Caza M, Lepine F, Dozois CM, Weiser JN. Klebsiella pneumoniae yersiniabactin promotes respiratory tract infection through evasion of lipocalin 2. Infect Immun. 2011;79:3309–16.PubMedPubMedCentralCrossRef
56.
Merlet A, Cazanave C, Dutronc H, de Barbeyrac B, Brisse S, Dupon M. Primary liver abscess due to CC23-K1 virulent clone of Klebsiella pneumoniae in France. Clin Microbiol Infect. 2012;18:E338–9.PubMedCrossRef
57.
58.
Pomakova DK, Hsiao CB, Beanan JM, Olson R, MacDonald U, Keynan Y, Russo TA. Clinical and phenotypic differences between classic and hypervirulent Klebsiella pneumonia: an emerging and under-recognized pathogenic variant. Eur J Clin Microbiol Infect Dis. 2012;31:981–9.PubMedCrossRef
59.
Russo TA, Shon AS, Beanan JM, Olson R, MacDonald U, Pomakov AO, Visitacion MP. Hypervirulent K. pneumoniae secretes more and more active iron-acquisition molecules than “classical” K. pneumoniae thereby enhancing its virulence. PLoS ONE. 2011;6:e26734.PubMedPubMedCentralCrossRef
60.
Sachdev DD, Yin MT, Horowitz JD, Mukkamala SK, Lee SE, Ratner AJ. Klebsiella pneumoniae K1 liver abscess and septic endophthalmitis in a U.S. resident. J Clin Microbiol. 2013;51:1049–51.PubMedPubMedCentralCrossRef
61.
Shon AS, Russo TA. Hypervirulent Klebsiella pneumoniae: the next superbug? Future Microbiol. 2012;7:669–71.PubMedCrossRef
62.
Fang CT, Chuang YP, Shun CT, Chang SC, Wang JT. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. J Exp Med. 2004;199:697–705.PubMedPubMedCentralCrossRef
63.
Lee CH, Liu JW, Su LH, Chien CC, Li CC, Yang KD. Hypermucoviscosity associated with Klebsiella pneumoniae-mediated invasive syndrome: a prospective cross-sectional study in Taiwan. Int J Infect Dis. 2010;14:e688–92.PubMedCrossRef
64.
Krapp F, Morris AR, Ozer EA, Hauser AR. Virulence characteristics of carbapenem-resistant Klebsiella pneumoniae strains from patients with necrotizing skin and soft tissue infections. Sci Rep. 2017;7:13533.PubMedPubMedCentralCrossRef
65.
Zhang Y, Zhao C, Wang Q, Wang X, Chen H, Li H, Zhang F, Li S, Wang R, Wang H. High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics, and antimicrobial resistance. Antimicrob Agents Chemother. 2016;60:6115–20.PubMedPubMedCentralCrossRef
66.
Harada S, Doi Y. Hypervirulent Klebsiella pneumoniae: a Call for Consensus Definition and International Collaboration. J Clin Microbiol. 2018;56.
67.
Karlsson M, Stanton RA, Ansari U, McAllister G, Chan MY, Sula E, Grass JE, Duffy N, Anacker ML, Witwer ML, Rasheed JK, Elkins CA, Halpin AL. Identification of a carbapenemase-producing hypervirulent Klebsiella pneumoniae isolate in the United States. Antimicrob Agents Chemother. 2019;63.
68.
Liu C, Du P, Xiao N, Ji F, Russo TA, Guo J. Hypervirulent Klebsiella pneumoniae is emerging as an increasingly prevalent K. pneumoniae pathotype responsible for nosocomial and healthcare-associated infections in Beijing, China. Virulence. 2020;11:1215–24.PubMedPubMedCentralCrossRef
69.
Wyres KL, Nguyen TNT, Lam MMC, Judd LM, van Vinh CN, Dance DAB, Ip M, Karkey A, Ling CL, Miliya T, Newton PN, Lan NPH, Sengduangphachanh A, Turner P, Veeraraghavan B, Vinh PV, Vongsouvath M, Thomson NR, Baker S, Holt KE. Genomic surveillance for hypervirulence and multi-drug resistance in invasive Klebsiella pneumoniae from South and Southeast Asia. Genome Med. 2020;12:11.PubMedPubMedCentralCrossRef
70.
Leverstein-van Hall MA, Fluit AC, Paauw A, Box AT, Brisse S, Verhoef J. Evaluation of the Etest ESBL and the BD Phoenix, VITEK 1, and VITEK 2 automated instruments for detection of extended-spectrum beta-lactamases in multiresistant Escherichia coli and Klebsiella spp. J Clin Microbiol. 2002;40:3703–11.PubMedPubMedCentralCrossRef
71.
Suravaram S, Hada V, Ahmed SI. Comparison of antimicrobial susceptibility interpretation among Enterobacteriaceae using CLSI and EUCAST breakpoints. Indian J Med Microbiol. 2021;39:315–9.PubMedCrossRef
72.
Heil EL, Johnson JK. Impact of CLSI breakpoint changes on microbiology laboratories and antimicrobial stewardship programs. J Clin Microbiol. 2016;54:840–4.PubMedPubMedCentralCrossRef
73.
Huang CC, Chen YS, Toh HS, Lee YL, Liu YM, Ho CM, Lu PL, Liu CE, Chen YH, Wang JH, Tang HJ, Yu KW, Liu YC, Chuang YC, Xu Y, Ni Y, Ko WC, Hsueh PR. Impact of revised CLSI breakpoints for susceptibility to third-generation cephalosporins and carbapenems among Enterobacteriaceae isolates in the Asia-Pacific region: results from the Study for Monitoring Antimicrobial Resistance Trends (SMART), 2002–2010. Int J Antimicrob Agents. 2012;40(Suppl):S4-10.PubMedCrossRef
74.
75.
Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes De Novo Assembler. Curr Protoc Bioinformatics. 2020;70: e102.PubMed
76.
Cherny KE, Ozer EA, Kochan TJ, Kociolek LK. Complete genome sequence of Clostridium innocuum Strain ATCC 14501. Microbiol Resour Announc. 2020;9.
77.
Cherny KE, Ozer EA, Kochan TJ, Johnson S, Kociolek LK. Complete genome sequence of Clostridium innocuum strain LC-LUMC-CI-001, isolated from a patient with recurrent antibiotic-associated diarrhea. Microbiol Resour Announc. 2020; 9.
78.
79.
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24.PubMedPubMedCentralCrossRef
80.
81.
Walker KA, Miller VL. The intersection of capsule gene expression, hypermucoviscosity and hypervirulence in Klebsiella pneumoniae. Curr Opin Microbiol. 2020;54:95–102.PubMedPubMedCentralCrossRef
82.
83.
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6.PubMedPubMedCentralCrossRef
84.
Wick RR, Heinz E, Holt KE, Wyres KL. Kaptive Web: user-friendly capsule and lipopolysaccharide serotype prediction for Klebsiella Genomes. J Clin Microbiol. 2018; 56.
85.
Robertson J, Nash JHE. 2018. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom. 2018; 4.
86.
87.
Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, Phillippy AM. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016;17:132.PubMedPubMedCentralCrossRef
88.
Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, Moller Aarestrup F, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895–903.PubMedPubMedCentralCrossRef
89.
90.
Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, Jenney A, Connor TR, Hsu LY, Severin J, Brisse S, Cao H, Wilksch J, Gorrie C, Schultz MB, Edwards DJ, Nguyen KV, Nguyen TV, Dao TT, Mensink M, Minh VL, Nhu NT, Schultsz C, Kuntaman K, Newton PN, Moore CE, Strugnell RA, Thomson NR. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA. 2015;112:E3574–81.PubMedPubMedCentral
91.
Conlan S, Park M, Deming C, Thomas PJ, Young AC, Coleman H, Sison C, Program NCS, Weingarten RA, Lau AF, Dekker JP, Palmore TN, Frank KM, Segre JA. Plasmid dynamics in KPC-positive Klebsiella pneumoniae during long-term patient colonization. mBio. 2016; 7.
92.
Lawlor MS, O’Connor C, Miller VL. Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection. Infect Immun. 2007;75:1463–72.PubMedPubMedCentralCrossRef
93.
Marsh JW, Mustapha MM, Griffith MP, Evans DR, Ezeonwuka C, Pasculle AW, Shutt KA, Sundermann A, Ayres AM, Shields RK, Babiker A, Cooper VS, Van Tyne D, Harrison LH. Evolution of outbreak-causing carbapenem-resistant Klebsiella pneumoniae ST258 at a Tertiary Care Hospital over 8 Years. mBio 2019;10.
94.
Yu WL, Lee MF, Tang HJ, Chang MC, Chuang YC. Low prevalence of rmpA and high tendency of rmpA mutation correspond to low virulence of extended spectrum beta-lactamase-producing Klebsiella pneumoniae isolates. Virulence. 2015;6:162–72.PubMedPubMedCentralCrossRef
95.
Rodrigues C, d'Humieres C, Papin G, Passet V, Ruppe E, Brisse S. Community-acquired infection caused by the uncommon hypervirulent Klebsiella pneumoniae ST66-K2 lineage. Microb Genom. 2020;6.
96.
Agard MJ, Ozer EA, Morris AR, Piseaux R, Hauser AR. A genomic approach to identify Klebsiella pneumoniae and acinetobacter baumannii strains with enhanced competitive fitness in the lungs during multistrain pneumonia. Infect Immun. 2019;87.
97.
Russo TA, Olson R, Macdonald U, Metzger D, Maltese LM, Drake EJ, Gulick AM. Aerobactin mediates virulence and accounts for increased siderophore production under iron-limiting conditions by hypervirulent (hypermucoviscous) Klebsiella pneumoniae. Infect Immun. 2014;82:2356–67.PubMedPubMedCentralCrossRef
98.
Kamau E, Allyn PR, Beaird OE, Ward KW, Kwan N, Garner OB, Yang S. Endogenous endophthalmitis caused by ST66-K2 hypervirulent Klebsiella pneumoniae, United States. Emerg Infect Dis. 2021;27:2215–8.PubMedPubMedCentralCrossRef
99.
Klaper K, Wendt S, Lubbert C, Lippmann N, Pfeifer Y, Werner G. Hypervirulent Klebsiella pneumoniae of Lineage ST66-K2 Caused Tonsillopharyngitis in a German Patient. Microorganisms 2021; 9.
100.
Russo TA, MacDonald U. The Galleria mellonella infection model does not accurately differentiate between hypervirulent and classical Klebsiella pneumoniae. mSphere 2020;5.
101.
Huang Y, Rana AP, Wenzler E, Ozer EA, Krapp F, Bulitta JB, Hauser AR, Bulman ZP. Aminoglycoside-resistance gene signatures are predictive of aminoglycoside MICs for carbapenem-resistant Klebsiella pneumoniae. J Antimicrob Chemother. 2022;77:356–63.PubMedCrossRef
102.
Ernst CM, Braxton JR, Rodriguez-Osorio CA, Zagieboylo AP, Li L, Pironti A, Manson AL, Nair AV, Benson M, Cummins K, Clatworthy AE, Earl AM, Cosimi LA, Hung DT. Adaptive evolution of virulence and persistence in carbapenem-resistant Klebsiella pneumoniae. Nat Med. 2020;26:705–11.PubMedPubMedCentralCrossRef
103.
Han SH. Review of hepatic abscess from Klebsiella pneumoniae. An association with diabetes mellitus and septic endophthalmitis. West J Med. 1995;162:220–4.PubMedPubMedCentral
104.
Huang CR, Lu CH, Chang HW, Lee PY, Lin MW, Chang WN. Community-acquired spontaneous bacterial meningitis in adult diabetic patients: an analysis of clinical characteristics and prognostic factors. Infection. 2002;30:346–50.PubMedCrossRef
105.
Wang JH, Liu YC, Lee SS, Yen MY, Chen YS, Wang JH, Wann SR, Lin HH. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis. 1998;26:1434–8.PubMedCrossRef
106.
Martin MJ, Corey BW, Sannio F, Hall LR, MacDonald U, Jones BT, Mills EG, Harless C, Stam J, Maybank R, Kwak Y, Schaufler K, Becker K, Hubner NO, Cresti S, Tordini G, Valassina M, Cusi MG, Bennett JW, Russo TA, McGann PT, Lebreton F, Docquier JD. Anatomy of an extensively drug-resistant Klebsiella pneumoniae outbreak in Tuscany, Italy. Proc Natl Acad Sci USA. 2021; 118.
107.
Heiden SE, Hubner NO, Bohnert JA, Heidecke CD, Kramer A, Balau V, Gierer W, Schaefer S, Eckmanns T, Gatermann S, Eger E, Guenther S, Becker K, Schaufler K. A Klebsiella pneumoniae ST307 outbreak clone from Germany demonstrates features of extensive drug resistance, hypermucoviscosity, and enhanced iron acquisition. Genome Med. 2020;12:113.PubMedPubMedCentralCrossRef
108.
Lambregts MMC, Wijnakker R, Bernards AT, Visser LG, Cessie SL, Boer MGJ. Mortality after delay of adequate empiric antimicrobial treatment of bloodstream infection. J Clin Med. 2020; 9.
109.
Weiss SL, Fitzgerald JC, Balamuth F, Alpern ER, Lavelle J, Chilutti M, Grundmeier R, Nadkarni VM, Thomas NJ. Delayed antimicrobial therapy increases mortality and organ dysfunction duration in pediatric sepsis. Crit Care Med. 2014;42:2409–17.PubMedPubMedCentralCrossRef
110.
Xiao SZ, Wang S, Wu WM, Zhao SY, Gu FF, Ni YX, Guo XK, Qu JM, Han LZ. The resistance phenotype and molecular epidemiology of Klebsiella pneumoniae in bloodstream infections in Shanghai, China, 2012–2015. Front Microbiol. 2017;8:250.PubMedPubMedCentral
111.
Kim YK, Pai H, Lee HJ, Park SE, Choi EH, Kim J, Kim JH, Kim EC. Bloodstream infections by extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in children: epidemiology and clinical outcome. Antimicrob Agents Chemother. 2002;46:1481–91.PubMedPubMedCentralCrossRef
112.
Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother. 2003;47:3724–32.PubMedPubMedCentralCrossRef
113.
Marra AR, Wey SB, Castelo A, Gales AC, Cal RG, Filho JR, Edmond MB, Pereira CA. Nosocomial bloodstream infections caused by Klebsiella pneumoniae: impact of extended-spectrum beta-lactamase (ESBL) production on clinical outcome in a hospital with high ESBL prevalence. BMC Infect Dis. 2006;6:24.PubMedPubMedCentralCrossRef
114.
Tumbarello M, Spanu T, Sanguinetti M, Citton R, Montuori E, Leone F, Fadda G, Cauda R. Bloodstream infections caused by extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae: risk factors, molecular epidemiology, and clinical outcome. Antimicrob Agents Chemother. 2006;50:498–504.PubMedPubMedCentralCrossRef
115.
Xu M, Fu Y, Kong H, Chen X, Chen Y, Li L, Yang Q. Bloodstream infections caused by Klebsiella pneumoniae: prevalence of blaKPC, virulence factors and their impacts on clinical outcome. BMC Infect Dis. 2018;18:358.PubMedPubMedCentralCrossRef
116.
117.
Weiner-Lastinger LM, Abner S, Benin AL, Edwards JR, Kallen AJ, Karlsson M, Magill SS, Pollock D, See I, Soe MM, Walters MS, Dudeck MA. Antimicrobial-resistant pathogens associated with pediatric healthcare-associated infections: summary of data reported to the National Healthcare Safety Network, 2015–2017. Infect Control Hosp Epidemiol. 2020;41:19–30.PubMedCrossRef
118.
Andrade LN, Vitali L, Gaspar GG, Bellissimo-Rodrigues F, Martinez R, Darini AL. Expansion and evolution of a virulent, extensively drug-resistant (polymyxin B-resistant), QnrS1-, CTX-M-2-, and KPC-2-producing Klebsiella pneumoniae ST11 international high-risk clone. J Clin Microbiol. 2014;52:2530–5.PubMedPubMedCentralCrossRef
119.
van Duin D, Arias CA, Komarow L, Chen L, Hanson BM, Weston G, Cober E, Garner OB, Jacob JT, Satlin MJ, Fries BC, Garcia-Diaz J, Doi Y, Dhar S, Kaye KS, Earley M, Hujer AM, Hujer KM, Domitrovic TN, Shropshire WC, Dinh A, Manca C, Luterbach CL, Wang M, Paterson DL, Banerjee R, Patel R, Evans S, Hill C, Arias R, Chambers HF, Fowler VG Jr, Kreiswirth BN, Bonomo RA, Multi-Drug Resistant Organism Network I. Molecular and clinical epidemiology of carbapenem-resistant Enterobacterales in the USA (CRACKLE-2): a prospective cohort study. Lancet Infect Dis. 2020;20:731–41.PubMedPubMedCentralCrossRef
120.
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. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. Proc Natl Acad Sci U S A. 2014;111:4988–93.PubMedPubMedCentralCrossRef
Metadata
Title
Genomic surveillance for multidrug-resistant or hypervirulent Klebsiella pneumoniae among United States bloodstream isolates
Authors
Travis J. Kochan
Sophia H. Nozick
Rachel L. Medernach
Bettina H. Cheung
Samuel W. M. Gatesy
Marine Lebrun-Corbin
Sumitra D. Mitra
Natalia Khalatyan
Fiorella Krapp
Chao Qi
Egon A. Ozer
Alan R. Hauser
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-022-07558-1

Other articles of this Issue 1/2022

BMC Infectious Diseases 1/2022 Go to the issue

Research

Multidrug resistant bacterial infections in severely ill COVID-19 patients admitted in a national referral and teaching hospital, Kenya

Research

Test concordance and diagnostic accuracy of three serological assays for detection of anti-SARS-CoV-2 antibody: result from a population-based sero-epidemiological study in Delhi

Research article

Discriminant models for the prediction of postponed viral shedding time and disease progression in COVID-19

Research article

Indirect comparison of 48-week efficacy and safety of long-acting cabotegravir and rilpivirine maintenance every 8 weeks with daily oral standard of care antiretroviral therapy in participants with virologically suppressed HIV-1-infection

Study protocol

Resistance to single dose albendazole and reinfection with intestinal helminths among children ages 2 to 11 years from the Peruvian Amazon region: a study protocol

Research

Testing and vaccination to reduce the impact of COVID-19 in nursing homes: an agent-based approach
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits