Bacteriological characteristics of hypervirulent Klebsiella pneumoniae rmpA gene (hvKp-rmpA)-harboring strains in the south of Iran
Abstract
Background and Objectives: To provide data on the occurrence of classical K. pneumoniae (cKp) and hypervirulent Klebsiella pneumoniae (hvKp) strains harboring the gene encoding regulator of mucoid phenotype A (rmpA) and evaluated characteristics of virulence biomarkers, carbapenemase, extended-spectrum-β-lactamase (ESBL)-producing, and capsule serotypes among K. pneumoniae clinical isolates collected in the south of Iran.
Materials and Methods: A total of 400 K. pneumoniae isolates were collected. First, the K. pneumoniae isolates were screened for rmpA gene by PCR, and then they were characterized for the presence of the virulence genes (pagO, iucA, iroB, luxR), capsular serotype genes (K1, K2, K5, K20, K54, and K57), carbapenemase (blaNDM, blaIMP, blaVIM, blaKPC, blaSPM, blaOXA-48, and blaOXA-181) and ESBL (blaCTX-M, blaSHV and blaTEM) genes. For all K. pneumoniae isolates phenotypic tests include of string test and disk diffusion test were performed.
Results: In total, 16 (4%) hvKp-rmpA+ and 384 (96%) cKp were observed. Of hvKp-rmpA+ strains, 16 (100%) were carried pagO, iroB, and luxR genes, and 13 (81.3%) strains harbored iucA gene. The most prevalent capsular type genes were K1 (62%) and K2 (19%) in hvKp-rmpA+ strains. The incidence of blaSHV gene in hvKp and cKp was 94% (15/16) and 87.5% (336/384), respectively. The cKp isolates carried blaNDM (30/384; 7.8%) gene.
Conclusion: Our data suggest that the incidence of hvKp was low. Also, hvKp-rmpA+ strains have less antibiotic resistance than cKp isolates. Serotypes K1 and K2, and blaSHV gene were strongly associated with hvKp-rmpA+.
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11. Feng Y, Lu Y, Yao Z, Zong Z. Carbapenem-resistant hypervirulent Klebsiella pneumoniae of sequence type 36. Antimicrob Agents Chemother 2018; 62(7): e02644-17.
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16. Nadasy KA, Domiati-Saad R, Tribble MA. Invasive Klebsiella pneumoniae syndrome in North America. Clin Infect Dis 2007; 45(3): e25-28.
17. Ye M, Tu J, Jiang J, Bi Y, You W, Zhang Y, et al. Clinical and genomic analysis of liver abscess-causing Klebsiella pneumoniae identifies new liver abscess-associated virulence genes. Front Cell Infect Microbiol 2016; 6: 165.
18. 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: 284-293.
19. Turton JF, Baklan H, Siu LK, Kaufmann ME, Pitt TL. Evaluation of a multiplex PCR for detection of serotypes K1, K2 and K5 in Klebsiella sp. and comparison of isolates within these serotypes. FEMS Microbiol Lett 2008; 284: 247-252.
20. Dallenne C, Da Costa A, Decre D, Favier C, Arle G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
21. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70: 119-123.
22. Lascols C, Hackel M, Marshall SH, Hujer AM, Bouchillon S, Badal R, et al. Increasing prevalence and dissemination of NDM-1 metallo-β-lactamase in India: data from the SMART study (2009). J Antimicrob Chemother 2011; 66: 1992-1997.
23. Potron A, Nordmann P, Lafeuille E, Maskari ZA, Rashdi FA, Poirel L. Characterization of OXA-181, a carbapenem-hydrolyzing class D beta-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemother 2011; 55: 4896-4899.
24. Corbellini S, Caccuri F, Gelmi M, De Francesco MA, Fiorentini S, Caruso A, et al. Emergence of carbapenem-resistant Klebsiella Pneumoniae strains producing KPC-3 in Brescia Hospital, Italy. New Microbiol 2014; 37: 177-183.
25. Li L, Yuan Z, Chen D, Xie X, Zhang B. Clinical and microbiological characteristics of invasive and hypervirulent Klebsiella pneumoniae infections in a teaching hospital in China. Infect Drug Resist 2020; 13: 4395-4403.
26. Liu C, Guo J. Hypervirulent Klebsiella pneumoniae (hypermucoviscous and aerobactin positive) infection over 6 years in the elderly in China: antimicrobial resistance patterns, molecular epidemiology and risk factor. Ann Clin Microbiol Antimicrob 2019; 18: 4.
27. Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U, et al. Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from classical K. J Clin Microbiol 2018; 56(9): e00776-18.
28. Taraghian A, Nasr Esfahani B, Moghim S, Fazeli H. Characterization of hypervirulent extended-spectrum β-Lactamase-producing Klebsiella pneumoniae among urinary tract infections: the first report from Iran. Infect Drug Resist 2020; 13: 3103-3111.
29. Tabrizi AMA, Badmasti F, Shahcheraghi F, Azizi O. Outbreak of hypervirulent Klebsiella pneumoniae harbouring blaVIM-2 among mechanically-ventilated drug-poisoning patients with high mortality rate in Iran. J Glob Antimicrob Resist 2018; 15: 93-98.
30. Alizade H, Jajarmi M, Aflatoonian MR, Kalantar-Neyestanaki D, Shoja S, Ghanbarpour R. Comparative Prevalence of blaCTX-M-15 Gene with Virulence Genes and Serotypes in Klebsiella pneumoniae. Jundishapur J Microbiol 2018; 11(4): e61285.
31. Catalán-Nájera JC, Garza-Ramos U, Barrios-Camacho H. Hypervirulence and hypermucoviscosity: Two different but complementary Klebsiella spp. phenotypes? Virulence 2017; 8: 1111-1123.
32. El-Mahdy R, El-Kannishy G, Salama H. Hypervirulent Klebsiella pneumoniae as a hospital-acquired pathogen in the intensive care unit in Mansoura, Egypt. Germs 2018; 8: 140-146.
33. Yan Q, Zhou M, Zou M, Liu WE. Hypervirulent Klebsiella pneumoniae induced ventilator-associated pneumonia in mechanically ventilated patients in China. Eur J Clin Microbiol Infect Dis 2016; 35: 387-396.
34. Zhang Y, Zhao C, Wang Q, Wang X, Chen H, Li H, et al. High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics and antimicrobial resistance. Antimicrob Agents Chemother 2016; 60: 6115-6120.
35. Guo Y, Wang S, Zhan L, Jin Y, Duan J, Hao Z, et al. Microbiological and clinical characteristics of hypermucoviscous Klebsiella pneumoniae isolates associated with invasive infections in China. Front Cell Infect Microbiol 2017; 7: 24.
36. Liu C, Shi J, Guo J. High prevalence of hypervirulent Klebsiella pneumoniae infection in the genetic background of elderly patients in two teaching hospitals in China. Infect Drug Resist 2018; 11: 1031-1041.
37. Sun Y, Wu H, Shen D. Clinical and molecular analysis of Klebsiella pneumoniae causing liver abscess in China. J Mol Microbiol Biotechnol 2016; 26: 245-251.
38. Lam MMC, Wyres KL, Duchêne S, Wick RR, Judd LM, Gan YH, et al. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat Commun 2018; 9: 2703.
39. Hernández M, López-Urrutia L, Abad D, De Frutos Serna M, Ocampo-Sosa AA, Eiros JM. First report of an extensively drug-resistant ST23 Klebsiella pneumoniae of capsular serotype k1 co-producing CTX-M-15, OXA-48 and ArmA in Spain. Antibiotics (Basel) 2021; 10: 157.
40. Parrott AM, Shi J, Aaron J, Green DA, Whittier S, Wu F. Detection of multiple hypervirulent Klebsiella pneumoniae strains in a New York City hospital through screening of virulence genes. Clin Microbiol Infect 2021; 27: 583-589.
2. Pajand O, Darabi N, Arab M, Ghorbani R, Bameri Z, Ebrahimi A, et al. The emergence of the hypervirulent Klebsiella pneumoniae (hvKp) strains among circulating clonal complex 147 (CC147) harbouring blaNDM/OXA‑48 carbapenemases in a tertiary care center of Iran. Ann Clin Microbiol Antimicrob 2020; 19: 12.
3. Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 2019; 32(3): e00001-19.
4. Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiol Mol Biol Rev 2016; 80: 629-661.
5. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 2015; 112(27): E3574- E3581.
6. Lin ZW, Zheng JX, Bai B, Xu GJ, Lin FJ, Chen Z, et al. Characteristics of Hypervirulent Klebsiella pneumoniae: does low expression of rmpA contribute to the absence of Hypervirulence? Front Microbiol 2020; 11: 436.
7. 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: 1215-1224.
8. Lee CR, Lee JH, Park KS, Jeon JH, Kim YB, Cha CJ, et al. Antimicrobial resistance of hypervirulent Klebsiella pneumoniae: epidemiology, hypervirulence-associated determinants, and resistance mechanisms. Front Cell Infect Microbiol 2017; 7: 483.
9. Kazemian H, Heidari H, Ghanavati R, Ghafourian S, Yazdani F, Sadeghifard N, et al. Phenotypic and genotypic characterization of ESBL-, AmpC-, and Carbapenemase-producing Klebsiella pneumoniae and Escherichia coli isolates. Med Princ Pract 2019; 28: 547-551.
10. Lee CH, Su LH, Tang YF, Liu JW. Treatment of ESBL-producing Klebsiella pneumoniae bacteraemia with carbapenems or flomoxef: a retrospective study and laboratory analysis of the isolates. J Antimicrob Chemother 2006; 58: 1074-1077.
11. Feng Y, Lu Y, Yao Z, Zong Z. Carbapenem-resistant hypervirulent Klebsiella pneumoniae of sequence type 36. Antimicrob Agents Chemother 2018; 62(7): e02644-17.
12. Mataseje LF, Boyd DA, Mulvey MR, Longtin Y. Two hypervirulent Klebsiella pneumoniae isolates producing a blaKPC-2 carbapenemase from a Canadian patient. Antimicrob Agents Chemother 2019; 63(7): e00517-19.
13. Winn Washington C, Allen SD, Janda WM, Koneman EW, Procop GW, Schreckenberger PC, et al. Koneman’s Color Atlas and Textbook of Diagnostic Microbiolgy. Lippincott, Williams & Wilkins, Philadelphia. 2006.
14. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; 30th informational supplement, CLSI document M100-S30. 2020. Clinical and Laboratory Standards Institute, Wayne, PA.
15. Shon AS, Bajwa RP, Russo TA. Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence 2013; 4: 107-118.
16. Nadasy KA, Domiati-Saad R, Tribble MA. Invasive Klebsiella pneumoniae syndrome in North America. Clin Infect Dis 2007; 45(3): e25-28.
17. Ye M, Tu J, Jiang J, Bi Y, You W, Zhang Y, et al. Clinical and genomic analysis of liver abscess-causing Klebsiella pneumoniae identifies new liver abscess-associated virulence genes. Front Cell Infect Microbiol 2016; 6: 165.
18. 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: 284-293.
19. Turton JF, Baklan H, Siu LK, Kaufmann ME, Pitt TL. Evaluation of a multiplex PCR for detection of serotypes K1, K2 and K5 in Klebsiella sp. and comparison of isolates within these serotypes. FEMS Microbiol Lett 2008; 284: 247-252.
20. Dallenne C, Da Costa A, Decre D, Favier C, Arle G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
21. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70: 119-123.
22. Lascols C, Hackel M, Marshall SH, Hujer AM, Bouchillon S, Badal R, et al. Increasing prevalence and dissemination of NDM-1 metallo-β-lactamase in India: data from the SMART study (2009). J Antimicrob Chemother 2011; 66: 1992-1997.
23. Potron A, Nordmann P, Lafeuille E, Maskari ZA, Rashdi FA, Poirel L. Characterization of OXA-181, a carbapenem-hydrolyzing class D beta-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemother 2011; 55: 4896-4899.
24. Corbellini S, Caccuri F, Gelmi M, De Francesco MA, Fiorentini S, Caruso A, et al. Emergence of carbapenem-resistant Klebsiella Pneumoniae strains producing KPC-3 in Brescia Hospital, Italy. New Microbiol 2014; 37: 177-183.
25. Li L, Yuan Z, Chen D, Xie X, Zhang B. Clinical and microbiological characteristics of invasive and hypervirulent Klebsiella pneumoniae infections in a teaching hospital in China. Infect Drug Resist 2020; 13: 4395-4403.
26. Liu C, Guo J. Hypervirulent Klebsiella pneumoniae (hypermucoviscous and aerobactin positive) infection over 6 years in the elderly in China: antimicrobial resistance patterns, molecular epidemiology and risk factor. Ann Clin Microbiol Antimicrob 2019; 18: 4.
27. Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U, et al. Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from classical K. J Clin Microbiol 2018; 56(9): e00776-18.
28. Taraghian A, Nasr Esfahani B, Moghim S, Fazeli H. Characterization of hypervirulent extended-spectrum β-Lactamase-producing Klebsiella pneumoniae among urinary tract infections: the first report from Iran. Infect Drug Resist 2020; 13: 3103-3111.
29. Tabrizi AMA, Badmasti F, Shahcheraghi F, Azizi O. Outbreak of hypervirulent Klebsiella pneumoniae harbouring blaVIM-2 among mechanically-ventilated drug-poisoning patients with high mortality rate in Iran. J Glob Antimicrob Resist 2018; 15: 93-98.
30. Alizade H, Jajarmi M, Aflatoonian MR, Kalantar-Neyestanaki D, Shoja S, Ghanbarpour R. Comparative Prevalence of blaCTX-M-15 Gene with Virulence Genes and Serotypes in Klebsiella pneumoniae. Jundishapur J Microbiol 2018; 11(4): e61285.
31. Catalán-Nájera JC, Garza-Ramos U, Barrios-Camacho H. Hypervirulence and hypermucoviscosity: Two different but complementary Klebsiella spp. phenotypes? Virulence 2017; 8: 1111-1123.
32. El-Mahdy R, El-Kannishy G, Salama H. Hypervirulent Klebsiella pneumoniae as a hospital-acquired pathogen in the intensive care unit in Mansoura, Egypt. Germs 2018; 8: 140-146.
33. Yan Q, Zhou M, Zou M, Liu WE. Hypervirulent Klebsiella pneumoniae induced ventilator-associated pneumonia in mechanically ventilated patients in China. Eur J Clin Microbiol Infect Dis 2016; 35: 387-396.
34. Zhang Y, Zhao C, Wang Q, Wang X, Chen H, Li H, et al. High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics and antimicrobial resistance. Antimicrob Agents Chemother 2016; 60: 6115-6120.
35. Guo Y, Wang S, Zhan L, Jin Y, Duan J, Hao Z, et al. Microbiological and clinical characteristics of hypermucoviscous Klebsiella pneumoniae isolates associated with invasive infections in China. Front Cell Infect Microbiol 2017; 7: 24.
36. Liu C, Shi J, Guo J. High prevalence of hypervirulent Klebsiella pneumoniae infection in the genetic background of elderly patients in two teaching hospitals in China. Infect Drug Resist 2018; 11: 1031-1041.
37. Sun Y, Wu H, Shen D. Clinical and molecular analysis of Klebsiella pneumoniae causing liver abscess in China. J Mol Microbiol Biotechnol 2016; 26: 245-251.
38. Lam MMC, Wyres KL, Duchêne S, Wick RR, Judd LM, Gan YH, et al. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat Commun 2018; 9: 2703.
39. Hernández M, López-Urrutia L, Abad D, De Frutos Serna M, Ocampo-Sosa AA, Eiros JM. First report of an extensively drug-resistant ST23 Klebsiella pneumoniae of capsular serotype k1 co-producing CTX-M-15, OXA-48 and ArmA in Spain. Antibiotics (Basel) 2021; 10: 157.
40. Parrott AM, Shi J, Aaron J, Green DA, Whittier S, Wu F. Detection of multiple hypervirulent Klebsiella pneumoniae strains in a New York City hospital through screening of virulence genes. Clin Microbiol Infect 2021; 27: 583-589.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10233 | |
| Keywords | ||
| Beta-lactamases; Carbapenem-resistant Enterobacteriaceae; Klebsiella pneumonia | ||
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How to Cite
1.
Shoja S, Ansari M, Bengar S, Rafiei A, Shamseddin J, Alizade H. Bacteriological characteristics of hypervirulent Klebsiella pneumoniae rmpA gene (hvKp-rmpA)-harboring strains in the south of Iran. Iran J Microbiol. 2022;14(4):475-483.
