Comparison of the pathogenic potential of Klebsiella pneumoniae isolates from human intestinal microbiota, surface waters, and sewage

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Introduction. Klebsiella pneumoniae, an opportunistic pathogen responsible for nosocomial and community-acquired infections, is present in soil and water. Still, the virulent potential of K. pneumoniae isolates from the environment is mostly unknown. Since isolates with multiple antibiotic resistance are currently considered to be the main threat of environmental pollution, the bulk of ecological studies of K. pneumoniae are devoted to the identification of just such isolates (mainly producers of beta-lactamases).

Material and methods. In this study, 42 isolates of K. pneumoniae isolated from wastewater, 19 from surface water sources, and 63 isolates from the intestinal microbiota of conventionally healthy cases were analyzed by PCR for the presence of potential virulence genes (ybts, kfu, rmpA, mrkD, K2 , alls, magA, iutA).

Results. As a result of the analysis, a statistically significant heterogeneity of the studied samples was revealed. Isolates from wastewater showed the highest proportion and spectrum of virulent genes (8 out of 8). Isolates from surface sources were statistically indistinguishable from isolates isolated from the intestinal microbiota of “conventionally healthy” people, while pathogenic determinants were also detected in these groups.

Conclusion. K. pneumoniae isolates from surface sources did not statistically differ from isolates from feces of “practically healthy” ones, although some of the virulent genes were also detected in these isolates. Wastewater can serve as a reservoir for highly virulent K. pneumoniae, to a greater extent than the intestines of healthy people, and can serve as a risk to public health. Additional studies with larger samples and a more comprehensive range of virulent traits are needed to predict the spread of hypervirulent strains.

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Galina Pay

Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency

编辑信件的主要联系方式.
Email: noemail@neicon.ru
ORCID iD: 0000-0001-7086-0899
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Daria Rakitina

Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency

Email: noemail@neicon.ru
ORCID iD: 0000-0003-3554-7690
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Marina Pankova

Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency

Email: noemail@neicon.ru
ORCID iD: 0000-0002-9133-3665
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Sergey Yudin

Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency

Email: noemail@neicon.ru
ORCID iD: 0000-0002-7942-8004
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Angelika Zagaynova

Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency

Email: angelikaangel@mail.ru
ORCID iD: 0000-0003-4772-9686

MD, Ph.D., Head of Microbiology and parasitology laboratory in the Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Biological Agency, Moscow, 119121, Russian Federation.

e-mail: mgoshin@cspmz.ru 

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参考

  1. Podschun R., Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 1998; 11(4): 589-603.
  2. Struve C., Krogfelt K.A. Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ. Microbiol. 2004; 6(6): 584-90. https://doi.org/10.1111/j.1462-2920.2004.00590.x
  3. Podschun R., Pietsch S., Höller C., Ullmann U. Incidence of Klebsiella species in surface waters and their expression of virulence factors. Appl. Environ. Microbiol. 2001; 67(7) 3325-7. https://doi.org/10.1128/aem.67.7.3325-3327.2001
  4. Choby J.E., Howard-Anderson J., Weiss D.S. Hypervirulent Klebsiella pneumoniae -clinical and molecular perspectives (Review). J. Intern. Med. 2020; 287: 283-300. https://doi.org/10.1111/joim.13007
  5. Lightfoot N. Bacteria of potential health concern. In: World Health Organization (WHO). Heterotrophic Plate Counts and Drinking-Water Safety. London; 2003: 61-79.
  6. Matsen J.M., Spindler J.A., Blosser R.O. Characterization of Klebsiella isolates from natural receiving waters and comparison with human isolates. Appl. Microbiol. 1974; 28(4): 672-8.
  7. Vasaikar S., Obi L., Morobe I., Bisi-Johnson M. Molecular characteristics and antibiotic resistance profiles of Klebsiella isolates in Mthatha, Eastern Cape Province, South Africa. Int. J. Microbiol. 2017; 2017: 8486742. https://doi.org/10.1155/2017/8486742
  8. Kim S.H., Wei C.I., Tzou Y.M., An H. Multidrug-resistant Klebsiella pneumoniae isolated from farm environments and retail products in Oklahoma. J. Food Prot. 2005; 68(10): 2022-9. https://doi.org/10.4315/0362-028x-68.10.2022
  9. Lee C.R., Lee J.H., Park K.S., Jeon J.H., Kim Y.B., Cha C.J., et al. Antimicrobial resistance of hypervirulent Klebsiella pneumoniae: epidemiology, hypervirulence-associated determinants, and resistance mechanisms. Front. Cell Infect. Microbiol. 2017; 7: 483. https://doi.org/10.3389/fcimb.2017.00483
  10. Fung C.P., Lin Y.T., Lin J.C., Chen T.L., Yeh K.M., Chang F.Y., et al. Klebsiella pneumoniae in gastrointestinal tract and pyogenic liver abscess. Emerg. Infect. Dis. 2012; 18(8): 1322-5. https://doi.org/10.3201/eid1808.111053
  11. Russo T.A., Olson R., Macdonald U., Metzger D., Maltese L.M., Drake E.J., et al. Aerobactin mediates virulence and accounts for increased siderophore production under iron-limiting conditions by hypervirulent (hypermucoviscous) Klebsiella pneumoniae. Infect. Immun. 2014; 82(6): 2356-67. https://doi.org/10.1128/IAI.01667-13
  12. Compain F., Babosan A., Brisse S., Genel N., Audo J., Ailloud F., et al. Multiplex PCR for detection of seven virulence factors and K1/K2 capsular serotypes of Klebsiella pneumoniae. J. Clin. Microbiol. 2014; 52(12): 4377-80. https://doi.org/10.1128/JCM.02316-14
  13. Analysis of arbitrary conjugacy tables using the chi-square criterion. Available at: https://medstatistic.ru/calculators/calchit.html (in Russian)
  14. Yu W.L., Ko W.C., Cheng K.C., Lee C.C., Lai C.C., Chuang Y.C. Comparison of prevalence of virulence factors for Klebsiella pneumoniae liver abscesses between isolates with capsular K1/K2 and non-K1/K2 serotypes. Diagn. Microbiol. Infect. Dis. 2008; 62(1): 1-6. https://doi.org/10.1016/j.diagmicrobio.2008.04.007
  15. Holden V.I., Breen P., Houle S., Dozois C.M., Bachman M.A. Klebsiella pneumoniae siderophores induce inflammation, bacterial dissemination, and HIF-1α stabilization during pneumonia. mBio. 2016; 7(5): e01397-16. https://doi.org/10.1128/mBio.01397-16
  16. Jagnow J., Clegg S. Klebsiella pneumoniae MrkD-mediated biofilm formation on extracellular matrix- and collagen-coated surfaces. Microbiology. 2003; 149(Pt. 9): 2397-405. https://doi.org/10.1099/mic.0.26434-0
  17. Murphy C., Clegg S. Klebsiella pneumoniae and type 3 fimbriae: nosocomial infection, regulation and biofilm formation. Future Microbiol. 2012; 7(8): 991-1002. https://doi.org/10.2217/fmb.12.74
  18. Chou H.C., Lee C.Z., Ma L.C., Fang C.T., Chang S.C., Wang J.T. Isolation of a chromosomal region of Klebsiella pneumoniae associated with allantoin metabolism and liver infection. Infect. Immun. 2004; 72(7): 3783-92. https://doi.org/10.1128/IAI.72.7.3783-3792.2004
  19. Bagley S.T. Habitat association of Klebsiella species. Infect. Control. 1985; 6(2): 52-8. https://doi.org/10.1017/s0195941700062603
  20. Huijbers P.M.C., Blaak H., De Jong M.C.M., Graat E.A.M., Vandenbroucke-Grauls C.M.J.E., De Roda Husman A.M. Role of the environment in the transmission of antimicrobial resistance to humans: a review. Environ. Sci. Technol. 2015; 49(20): 11993-2004. https://doi.org/10.1021/acs.est.5b02566
  21. Bréchet C., Plantin J., Sauget M., Thouverez M., Talon D., Cholley P., et al. Wastewater treatment plants release large amounts of extended-spectrum beta-lactamase-producing Escherichia coli into the environment. Clin. Infect. Dis. 2014; 58(12): 1658-65. https://doi.org/10.1093/cid/ciu190
  22. Ram B., Kumar M. Correlation appraisal of antibiotic resistance with fecal, metal and microplastic contamination in a tropical Indian river, lakes and sewage. npj Clean Water. 2020; 3: 3. https://doi.org/10.1038/s41545-020-0050-1
  23. Khan F.A., Hellmark B., Ehricht R., Söderquist B., Jass J. Related carbapenemase-producing Klebsiella isolates detected in both a hospital and associated aquatic environment in Sweden. Eur. J. Clin. Microbiol. Infect. Dis. 2018; 37(12): 2241-51. https://doi.org/10.1007/s10096-018-3365-9
  24. Mcarthur J.V., Tuckfield R.C. Spatial patterns in antibiotic resistance among stream bacteria: effects of industrial pollution. Appl. Environ. Microbiol. 2000; 66(9): 3722-6. https://doi.org/10.1128/aem.66.9.3722-3726.2000
  25. Graham D.W., Olivares-Rieumont S., Knapp C.W., Lima L., Werner D., Bowen E. Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana, Cuba. Environ. Sci. Technol. 2011; 45(2): 418-24. https://doi.org/10.1021/es102473z
  26. Lepuschitz S., Schill S., Stoeger A., Pekard-Amenitsch S., Huhulescu S., Inreiter N., et al. Whole genome sequencing reveals resemblance between ESBL-producing and carbapenem resistant Klebsiella pneumoniae isolates from Austrian rivers and clinical isolates from hospitals. Sci. Total Environ. 2019; 662: 227-35. https://doi.org/10.1016/j.scitotenv.2019.01.179
  27. Atmani S.M., Messai Y., Alouache S., Fernandez R., Estepa V., Torres C., et al. Virulence characteristics and genetic background of ESBL-producing Klebsiella pneumoniae isolates from wastewater. Fresenius Environ. Bull. 2015; 24(1): 103-12.
  28. Runcharoen C., Moradigaravand D., Blane B., Paksanont S., Thammachote J., Anun S., et al. Whole genome sequencing reveals high-resolution epidemiological links between clinical and environmental Klebsiella pneumoniae. Genome Med. 2017; 9(1): 6. https://doi.org/10.1186/s13073-017-0397-1
  29. Surleac M., Czobor Barbu I., Paraschiv S., Popa L.I., Gheorghe I., Marutescu L., et al. Whole genome sequencing snapshot of multi-drug resistant Klebsiella pneumoniae strains from hospitals and receiving wastewater treatment plants in Southern Romania. PLoS One. 2020; 15(1): e0228079. https://doi.org/10.1371/journal.pone.0228079
  30. Barati A., Ghaderpour A., Chew L.L., Bong C.W., Thong K.L., Chong V.C., et al. Isolation and characterization of aquatic-borne Klebsiella pneumoniae from tropical estuaries in Malaysia. Int. J. Environ. Res. Public Health. 2016; 13(4): 426. https://doi.org/10.3390/ijerph13040426
  31. Mohammed E.S., Flayyih M.T. Detection of rmpA and magA genes and hypermucoviscosity phenotype in Klebsiella pneumoniae isolated from water samples in compare with clinical isolates. Curr. Res. Microbiol. Biotechnol. 2018; 6(1): 1424-30.
  32. Ko W.C., Paterson D.L., Sagnimeni A.J., Hansen D.S., Von Gottberg A., Mohapatra S., et al. Community-acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg. Infect. Dis. 2002; 8(2): 160-6. https://doi.org/10.3201/eid0802.010025

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版权所有 © Pay G.V., Rakitina D.V., Pankova M.N., Yudin S.M., Zagaynova A.V., 2020


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