Carbapenem-resistant klebsiella pneumoniae exhibit variability in capsular polysaccharide and capsule associated virulence traits

Journal of Infectious Diseases

Volumn 210, Issue 5, 2014, Pages 803-813

  Diago Navarro, Elizabeth ^a   Chen, Liang ^b   Passet, Virginie ^c,d   Burack, Seth ^a   Ulacia Hernando, Amaia ^a   Kodiyanplakkal, Rosy Priya ^a   Levi, Michael H ^e   Brisse, Sylvain ^c,d   Kreiswirth, Barry N ^b   Fries, Bettina C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

^e MONTEFIORE MEDICAL CENTER   (United States)

Author keywords

Adjuvant therapy; Carbapenem resistance; Klebsiella pneumoniae; Virulence

Indexed keywords

BACTERIAL POLYSACCHARIDE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 1C9; UNCLASSIFIED DRUG;

ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOCHEMICAL COMPOSITION; BIOFILM; CARBAPENEM RESISTANT KLEBSIELLA PNEUMONIAE; CELL KILLING; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; DISEASE ASSOCIATION; FEMALE; GALLERIA MELLONELLA; GENOTYPE; HUMAN; KLEBSIELLA PNEUMONIAE; MACROPHAGE; MALE; MOUSE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS;

ADJUVANT THERAPY; CARBAPENEM RESISTANCE; KLEBSIELLA PNEUMONIAE; VIRULENCE;

AGED; AGED, 80 AND OVER; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES, BACTERIAL; BACTERIAL CAPSULES; BETA-LACTAM RESISTANCE; BIOFILMS; BLOOD BACTERICIDAL ACTIVITY; CARBAPENEMS; FEMALE; GENOTYPE; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LEPIDOPTERA; MACROPHAGES; MALE; MICE, INBRED BALB C; MIDDLE AGED; MOLECULAR TYPING; RETROSPECTIVE STUDIES; SURVIVAL ANALYSIS; UNITED STATES; VIRULENCE;

EID: 84901282068     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu157     Document Type: Article

References (50)

1. Yigit H, Queenan AM, Anderson GJ, et al. Novel carbapenem-hydrolyzing beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother 2001; 45:1151-61.
2. (CDC) CfDCaP. Vital signs: carbapenem-resistant enterobacteriaceae. MMWR Morb Mortal Wkly Rep 2013; 62:165-70.
3. Kitchel B, Rasheed JK, Patel JB, et al. Molecular epidemiology of KPCproducing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother 2009; 53:3365-70.
4. Neuner EA, Yeh JY, Hall GS, et al. Treatment and outcomes in carbapenem- resistant Klebsiella pneumoniae bloodstream infections. Diagn Microbiol Infect Dis 2011; 69:357-62.
5. Hirsch EB, Tam VH. Detection and treatment options for Klebsiella pneumoniae carbapenemases (KPCs): an emerging cause of multidrug- resistant infection. J Antimicrob Chemother 2010; 65:1119-25.
6. Wernli D, Haustein T, Conly J, Carmeli Y, Kickbusch I, Harbarth S. A call for action: the application of The International Health Regulations to the global threat of antimicrobial resistance. PLoS Med 2011; 8:e1001022.
7. Cortes G, Borrell N, de Astorza B, Gomez C, Sauleda J, Alberti S. Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 2002; 70:2583-90.
8. Wu MF, Yang CY, Lin TL, et al. Humoral immunity against capsule polysaccharide protects the host from magA+ Klebsiella pneumoniaeinduced lethal disease by evading Toll-like receptor 4 signaling. Infect Immun 2009; 77:615-21.
9. Arakawa Y, Wacharotayankun R, Nagatsuka T, Ito H, Kato N, Ohta M. Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in the virulent strain Chedid. J Bacteriol 1995; 177:1788-96.
10. Brisse S, Issenhuth-Jeanjean S, Grimont PA. Molecular serotyping of Klebsiella species isolates by restriction of the amplified capsular antigen gene cluster. J Clin Microbiol 2004; 42:3388-98.
11. Brisse S, Passet V, Haugaard AB, et al. wzi gene sequencing, a rapid method to determine the capsular type of Klebsiella strains. J Clin Microbiol 2013; 51:4073-8.
12. 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.
13. Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005; 43:4178-82.
14. Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM, Snyd LR. Methods for General and Molecular Microbiology. 3rd Edition. Vol. ASM Press, 2007.
15. Cano V, Moranta D, Llobet-Brossa E, Bengoechea JA, Garmendia J. Klebsiella pneumoniae triggers a cytotoxic effect on airway epithelial cells. BMC Microbiol 2009; 9:156.
16. Merkle RK, Poppe I. Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol 1994; 230:1-15.
17. York WS, Darvill AG, McNeil M, Stevenson TT, Albersheim P. Isolation and characterization of plant cell walls and cell wall components. In: Arthur Weissbach HW, ed. Methods Enzymol. Vol. 118. Academic Press, 1986:3-40.
18. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 1998; 28:449-61.
19. Maldonado NC, de Ruiz CS, Cecilia M, Nader-Macias ME. A simple technique to detect Klebsiella biofilm-forming-strains. Inhibitory potential of Lactobacillus fermentum CRL 1058 whole cells and products. In: Méndez-Vilas A, ed. Communicating Current Research and Educational Topics and Trends in Applied Microbiology. Formatex, 2007.
20. Podschun R, Sievers D, Fischer A, Ullmann U. Serotypes, hemagglutinins, siderophore synthesis, and serum resistance of Klebsiella isolates causing human urinary tract infections. J Infect Dis 1993; 168:1415-21.
21. Belaaouaj A, McCarthy R, Baumann M, et al. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat Med 1998; 4:615-8.
22. Zdybicka-Barabas A, Cytrynska M. Involvement of apolipophorin III in antibacterial defense of Galleria mellonella larvae. Comp Biochem Physiol B Biochem Mol Biol 2011; 158:90-8.
23. Bhan U, Lukacs NW, Osterholzer JJ, et al. TLR9 is required for protective innate immunity in Gram-negative bacterial pneumonia: role of dendritic cells. J Immunol 2007; 179:3937-46.
24. Varshney AK, Wang X, Cook E, et al. Generation, characterization, and epitope mapping of neutralizing and protective monoclonal antibodies against staphylococcal enterotoxin B-induced lethal shock. J Biol Chem 2011; 286:9737-47.
25. CLSI. Performance standards for antimicrobial susceptibility testing. Twenty-third informational supplement. Wayne, PA: CLSI, 2013.
26. 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.
27. Satlin MJ, Calfee DP, Chen L, et al. Emergence of carbapenem-resistant Enterobacteriaceae as causes of bloodstream infections in patients with hematologic malignancies. Leuk Lymphoma 2013; 54:799-806.
28. Giske CG, Froding I, Hasan CM, et al. Diverse sequence types of Klebsiella pneumoniae contribute to the dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob Agents Chemother 2012; 56:2735-8.
29. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 2011; 35:736-55.
30. Vimont S, Mnif B, Fevre C, Brisse S. Comparison of PFGE and multilocus sequence typing for analysis of Klebsiella pneumoniae isolates. J Med Microbiol 2008; 57:1308-10.
31. Mataseje LF, Boyd DA, Willey BM, et al. Plasmid comparison and molecular analysis of Klebsiella pneumoniae harbouring bla(KPC) from New York City and Toronto. J Antimicrob Chemother 2011; 66:1273-7.
32. Kumar V, Sun P, Vamathevan J, et al. Comparative genomics of Klebsiella pneumoniae strains with different antibiotic resistance profiles. Antimicrob Agents Chemother 2011; 55:4267-76.
33. Snitkin ES, Zelazny AM, Thomas PJ, et al. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 2012; 4:148ra16.
34. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 1998; 11:589-603.
35. Kubler-Kielb J, Vinogradov E, Ng WI, et al. The capsular polysaccharide and lipopolysaccharide structures of two carbapenem resistant Klebsiella pneumoniae outbreak isolates. Carbohydr Res 2013; 369:6-9.
36. Brisse S, Fevre C, Passet V, et al. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 2009; 4:e4982.
37. Singh A, Tuteja U, Khushiramani R, Jain R, Batra HV. Generation and characterization of monoclonal antibodies against Klebsiella pneumoniae. Hybridoma (Larchmt) 2008; 27:199-203.
38. Lang AB, Bruderer U, Senyk G, Pitt TL, Larrick JW, Cryz SJ Jr. Human monoclonal antibodies specific for capsular polysaccharides of Klebsiella recognize clusters of multiple serotypes. J Immunol 1991; 146:3160-4.
39. Smith K, Muther JJ, Duke AL, et al. Fully human monoclonal antibodies from antibody secreting cells after vaccination with Pneumovax(R)23 are serotype specific and facilitate opsonophagocytosis. Immunobiology 2013; 218:745-54.
40. Fung CP, Chang FY, Lee SC, et al. A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis? Gut 2002; 50:420-4.
41. Fang CT, Lai SY, Yi WC, Hsueh PR, Liu KL, Chang SC. Klebsiella pneumoniae genotype K1: an emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clin Infect Dis 2007; 45:284-93.
42. Hsu CR, Lin TL, Chen YC, Chou HC, Wang JT. The role of Klebsiella pneumoniae rmpA in capsular polysaccharide synthesis and virulence revisited. Microbiology 2011; 157:3446-57.
43. Kong Q, Beanan JM, Olson R, et al. Biofilm formed by a hypervirulent (hypermucoviscous) variant of Klebsiella pneumoniae does not enhance serum resistance or survival in an in vivo abscess model. Virulence 2012; 3:309-18.
44. Serezani CH, Aronoff DM, Jancar S, Mancuso P, Peters-Golden M. Leukotrienes enhance the bactericidal activity of alveolar macrophages against Klebsiella pneumoniae through the activation of NADPH oxidase. Blood 2005; 106:1067-75.
45. Sahly H, Schubert S, Harder J, et al. Activity of human beta-defensins 2 and 3 against ESBL-producing Klebsiella strains. J Antimicrob Chemother 2006; 57:562-5.
46. Tsai WC, Strieter RM, Zisman DA, et al. Nitric oxide is required for effective innate immunity against Klebsiella pneumoniae. Infect Immun 1997; 65:1870-5.
47. Tzouvelekis LS, Miriagou V, Kotsakis SD, et al. KPC-producing, multidrug resistant Klebsiella pneumoniae ST258 as a typical opportunistic pathogen. Antimicrob Agents Chemother 2013; 57:5144-6.
48. March C, Cano V, Moranta D, et al. Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. PLoS One 2013; 8:e56847.
49. Insua JL, Llobet E, Moranta D, et al. Modelling Klebsiella pneumoniae pathogenesis by infecting the wax moth Galleria mellonella. Infect Immun 2013; 81:3552-65.
50. Romero-Steiner S, Frasch CE, Carlone G, Fleck RA, Goldblatt D, Nahm MH. Use of opsonophagocytosis for serological evaluation of pneumococcal vaccines. Clin Vaccine Immunol 2006; 13:165-9.