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Impairment of Respiratory Burst in Polymorphonuclear Leukocytes by Extended-Spectrum Beta-Lactamase-Producing Strains of Klebsiella pneumoniae

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Abstract

The ability of extended-spectrum β-lactamase (ESBL)-producing and non-ESBL-producing Klebsiella pneumoniae strains to induce a respiratory burst in polymorphonuclear leukocytes (PMNLs) was investigated. Ninety ESBL-producing and 178 non-ESBL-producing Klebsiella pneumoniae isolates were serotyped and their ability to induce a respiratory burst in PMNLs tested by monitoring the cells’ chemiluminescence (CL) response. The percentage of isolates inducing high levels of CL response (CL>75%) was significantly higher among non-ESBL producers (52%) than among ESBL producers (32.2%) (P<0.0001; OR=3.396; 95%CI=2.036–5.664). The median CL response was significantly higher among the non-ESBL producers (76.9%) than among the ESBL producers (52.6%) (P=0.034). The two groups did not differ in their ability to resist intracellular killing by PMNLs (P>0.05), with strains inducing high levels of CL response having significantly lower survival rates (31.8% vs. 42.4%) than strains inducing low levels of CL response (164% vs. 200%) (P<0.01). The frequencies of the K2 and the K25 serotypes were significantly higher among ESBL-producing strains (17.8% and 22.2%, respectively) than among the non-ESBL producers (6.2% and 1.7%, respectively) (P=0.0057 and P<0.0001). Of the 77 Klebsiella K serotypes, 71 were detectable among the non-ESBL producers, but only 24 were detectable among the ESBL producers. ESBL-producing Klebsiella pneumoniae strains might have a greater pathogenic potential by virtue of their ability to escape the phagocytic activity of PMNLs.

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References

  1. Sahly H, Podschun R, Ullmann U (2000) Klebsiella infections in the immunocompromised host. Adv Exp Med Biol 479:237–249

    CAS  PubMed  Google Scholar 

  2. Podschun R, Ullmann U (1998) Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 11:589–603

    CAS  PubMed  Google Scholar 

  3. Bradford PA (2001) Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 14:933–951

    Article  CAS  PubMed  Google Scholar 

  4. Jacoby G (1998) Epidemiology of extended-spectrum beta-lactamases. Clin Infect Dis 27:81–83

    CAS  PubMed  Google Scholar 

  5. Livermore D, Yuan M (1996) Antibiotic resistance and production of extended-spectrum β-lactamases amongst Klebsiella spp. from intensive care units in Europe. J Antimicrob Chemother 38:409–424

    CAS  PubMed  Google Scholar 

  6. Winokur PL, Canton R, Casellas JM, Legakis N (2001) Variations in the prevalence of strains expressing an extended-spectrum beta-lactamase phenotype and characterization of isolates from Europe, the Americas, and the Western Pacific region. Clin Infect Dis 32:94–103

    Article  Google Scholar 

  7. Cryz SJ, Fürer E, Germanier R (1984) Experimental Klebsiella pneumoniae burn wound sepsis: role of capsular polysaccharide. Infect Immun 43:440–441

    CAS  PubMed  Google Scholar 

  8. Domenico P, Johanson WG, Straus DC (1982) Lobar pneumonia in rats produced by clinical isolates of Klebsiella pneumoniae. Infect Immun 37:327–335

    CAS  PubMed  Google Scholar 

  9. Ehrenwort L, Baer H (1956) The pathogenicity of Klebsiella pneumoniae for mice: the relationship to the quantity and rate of production of type-specific capsular polysaccharide. J Bacteriol 72:713–717

    PubMed  Google Scholar 

  10. Highsmith AK, Jarvis WR (1985) Klebsiella pneumoniae: selected virulence factors that contribute to pathogenicity. Infect Control 6:75–77

    Google Scholar 

  11. Ofek I, Goldhar J, Keisari Y, Sharon N (1995) Nonopsonic phagocytosis of microorganisms. Ann Rev Microbiol 49:239–276

    Article  CAS  Google Scholar 

  12. Podschun R, Penner I, Ullmann U (1992) Interaction of Klebsiella capsular type 7 with human polymorphonuclear leucocytes. Microb Pathog 13:371–379

    CAS  PubMed  Google Scholar 

  13. Podschun R Ullmann U (1992) Klebsiella capsular type K7 in relation to toxicity, susceptibility to phagocytosis and resistance to serum. J Med Microbiol 36:250–254

    CAS  PubMed  Google Scholar 

  14. Simoons-Smit AM, Verweij-van Vught AMJJ, Kanis IYR, MacLaren DM (1985) Chemiluminescence of human leucocytes stimulated by clinical isolates of Klebsiella. J Med Microbiol 19:333–338

    CAS  PubMed  Google Scholar 

  15. Simoons-Smit AM, Verweij-van Vught AMJJ, D. MacLaren DM (1986) The role of K antigens as virulence factors in Klebsiella. J Med Microbiol 21:133–137

    CAS  PubMed  Google Scholar 

  16. Williams P, Tomas JM (1990) The pathogenicity of Klebsiella pneumoniae. Rev Med Microbiol 1:196–204

    Google Scholar 

  17. Ørskov I, Ørskov F (1984) Serotyping of Klebsiella. In: Bergan T (ed.) Methods in microbiology, vol 14. Academic Press, London, pp 143–164

  18. Darfeuille-Michaud A, Jallat C, Aubel D, Sirot D, Rich C, Sirot J, Joly B (1992) R-plasmid-encoded adhesive factor in Klebsiella pneumoniae strains responsible for human nosocomial infections. Infect Immun 60:44–45

    CAS  PubMed  Google Scholar 

  19. Di Martino P, Livrelli V, Sirot D, Joly B, Darfeuille-Michaud A (1996) A new fimbrial antigen harbored by CAZ-5/SHV-4-producing Klebsiella pneumoniae strains involved in nosocomial infections. Infect Immun 64:2266–2273

    PubMed  Google Scholar 

  20. Di Martino P, Sirot D, Joly B, Rich C, Darfeuille-Michaud A (1997) Relationship between adhesion to intestinal Caco-2 cells and multidrug resistance in Klebsiella pneumoniae clinical isolates. J Clin Microbiol 35:1499–1503

    PubMed  Google Scholar 

  21. Livrelli V, De Champ C, Di Martino P, Darfeuille-Michaud A, Forestier C, Joly B (1996) Adhesive properties and antibiotic resistance of Klebsiella, Enterobacter, and Serratia clinical isolates involved in nosocomial infections. J Clin Microbiol 34:1963–1969

    CAS  PubMed  Google Scholar 

  22. Sahly H, Aucken H, Benedi VJ, Forestier C, Hansen DS, Krogfelt K, Oelschlaeger T, Podschun R, Sirot D, Tomás JM, Ullmann U, Ofek I (2001) Association between extended-spectrum beta-lactamase production, O-serotypes and serum resistance properties in Klebsiella isolates from different European countries. Clin Microbiol Infect 7:286

    Google Scholar 

  23. Toivanen P, Hansen DS, Mestre F, Lehtonen L, Vaahtovuo J, Vehma M, Mottonen T, Saario R, Luukkainen R, Nissila M (1999) Somatic serogroups, capsular types, and species of fecal Klebsiella in patients with ankylosing spondylitis. J Clin Microbiol 37:2808–2812

    CAS  PubMed  Google Scholar 

  24. Jarlier V, Nicolas MH, Fournier G, Philippon A (1988) Extended broad-spectrum β-lactamases conferring transferable resistance to newer β-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis 10:867–878

    CAS  PubMed  Google Scholar 

  25. Hansen DS, Mestre F, Alberti S, Hernandez-Alles S, Alvarez D, Domenech-Sanchez A, Gil J, Merino S, Tomas JM, Benedi VJ (1999). Klebsiella pneumoniae lipopolysaccharide O typing: revision of prototype strains and O-group distribution among clinical isolates from different sources and countries. J Clin Microbiol 37:56–62

    CAS  PubMed  Google Scholar 

  26. Bruce J (1996) Automated system rapidly identifies and characterizes microorganisms in food. Food Technol 50:77–81

    Google Scholar 

  27. Hansen DS, Skov R, Benedí VJ, Sperling V, Kolmos HJ (2002) Klebsiella typing: pulsed-field gel electrophoresis (PFGE) in comparison with O:K serotyping. Clin Microbiol Infect 8:397–404

    Article  CAS  PubMed  Google Scholar 

  28. Falkow S (1997) Perspectives series: host/pathogen interactions. Invasion and intracellular sorting of bacteria: searching for bacterial genes expressed during host/pathogen interactions. J Clin Invest 100:239–243

    CAS  PubMed  Google Scholar 

  29. Tomas JM, Benedi VJ, Ciurana B, Jofre J (1986) Role of capsule and O antigen in resistance of Klebsiella pneumoniae to serum bactericidal activity. Infect Immun 54:85–89

    CAS  PubMed  Google Scholar 

  30. Williams P, Lambert PA, Brown MRW, Jones RJ (1983) The role of the O and K antigens in determining the resistance of Klebsiella aerogenes to serum killing and phagocytosis. J Gen Microbiol 129:2181–2191

    CAS  PubMed  Google Scholar 

  31. Podschun R, Greske B, Ullmann U (1994) Alternative and classical complement pathway activity of non-immune serum on Klebsiella serotypes K2, K7 and K55. In: Abstracts of the 6th International Congress for Infectious Diseases, Prague, Abstract no. 1363

  32. Casewell M, Talsania HG (1979) Predominance of certain Klebsiella capsular types in hospitals in the United Kingdom. J Infect 1:77–79

    Google Scholar 

  33. Podschun R, Heineken P, Ullmann U, Sonntag HG (1986) Comparative investigations of Klebsiella species of clinical origin: plasmid patterns, biochemical reactions, antibiotic resistances and serotypes. Zentralbl Bakteriol Hyg A 262:335–345

    CAS  Google Scholar 

  34. Podschun R (1990) Phenotypic properties of Klebsiella pneumoniae and K. oxytoca isolated from different sources. Zentralbl Hyg 189:527–535

    CAS  Google Scholar 

  35. Podschun R, Sievers D, Fischer A, Ullmann U (1993) Serotypes, hemagglutinins, siderophore synthesis, and serum resistance of Klebsiella isolates causing human urinary tract infections. J Infect Dis 168:1415–1421

    CAS  PubMed  Google Scholar 

  36. Riser E, Noone P (1981) Klebsiella capsular type versus site of isolation. J Clin Pathol 34:552–555

    CAS  PubMed  Google Scholar 

  37. Mizuta K, Ohta M, Mori M, Hasegawa T, Nakashima I, Kato N (1983) Virulence for mice of Klebsiella strains belonging to the O1 group: relationship to their capsule (K) types. Infect Immun 40:56–61

    CAS  PubMed  Google Scholar 

  38. Yuan M, Aucken H, Hall L, Pitt T, Livermore D (1998) Epidemiological typing of Klebsiellae with extended-spectrum beta-lactamases from European intensive care units. J Antimicrob Chemother 41:527–539

    Article  CAS  PubMed  Google Scholar 

  39. De Melo MC, Sa Figueiredo AM, Ferreira-Carvalho BT (2003) Antimicrobial susceptibility patterns and genomic diversity in strains of Streptococcus pyogenes isolated in 1978–1997 in different Brazilian cities. J Med Microbiol 52:251–258

    PubMed  Google Scholar 

  40. Tomasz A, Munoz R (1995) Beta-lactam antibiotic resistance in gram-positive bacterial pathogens of the upper respiratory tract: a brief overview of mechanisms. Microb Drug Resist 1:103–109

    CAS  PubMed  Google Scholar 

  41. Trick WE, Weinstein RA, DeMarais PL, Kuehnert MJ, Tomaska W, Nathan C, Rice TW, McAllister SK, Carson LA, Jarvis WR (2001) Colonization of skilled-care facility residents with antimicrobial-resistant pathogens. J Am Geriatr Soc 49:270–276

    Article  CAS  PubMed  Google Scholar 

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The experiments conducted in this study comply with the current laws of the countries in which they were performed.

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Correspondence to H. Sahly.

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This study is submitted in memory of Vicente Javier Benedi, who died prior to submission of the manuscript

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Sahly, H., Aucken, H., Benedi, V.J. et al. Impairment of Respiratory Burst in Polymorphonuclear Leukocytes by Extended-Spectrum Beta-Lactamase-Producing Strains of Klebsiella pneumoniae . Eur J Clin Microbiol Infect Dis 23, 20–26 (2004). https://doi.org/10.1007/s10096-003-1047-7

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