1887

Abstract

New Delhi metallo-β-lactamase (NDM)-producing has become a serious global health concern.

Due to the high genetic diversity among NDM-positive we need further surveillance and studies to better understand the relationships between them. In addition, the coexistence of several plasmid replicon types in NDM-positive may affect the copy number of , the MIC level to antibiotics, as well as increasing the chance of horizontal gene transfer.

The aim of this study was to determine incompatible plasmid groups and copy numbers of , and to investigate the genetic relationship of 37 NDM-positive in Kerman, Iran.

The gene was detected and confirmed by PCR-sequencing. The plasmid replicon types were determined by PCR-based replicon typing (PBRT) and the copy number of was determined by quantitaive real time-PCR (qPCR). Random amplified polymorphic DNA (RAPD)-PCR typing was used to detect genetic relationships between the strains.

In this study, 10 different replicon types, including Frep [=25 (67.5 %)], FIIAs [=11 (29.7 %)], FIA [=5 (13.5 %)], FIB [=3 (8.1 %)], I1-Iγ [=2 (5.4 %)], L/M [=7 (18.9 %)], A/C [=7 (18.9 %)], Y [=3 (8.1 %)], P [=1 (2.7 %)] and FIC [=1 (2.7 %)] were reported. The copy numbers of the gene varied from 30.00 to 5.0×10 and no statistically significant correlation was observed between a rise of the MIC to imipenem and the copy numbers of (>0.05). According to RAPD typing results, 35 strains were divided into five clusters, while two strains were non-typeable.

The spread of NDM-1-producing strains that carry several plasmid replicon types increases the chance of horizontal transfer of antibiotic resistance genes in hospital settings. In this study, 10 different replicon types were identified. We could not find any relationship between the increase of MIC levels to imipenem and the copy numbers of . Therefore, due to the identification of different replicon types in this study, the type and genetic characteristics of -carrying plasmids, and other factors such as antibiotic selective pressure, probably affect the copy number of and change the MIC level to imipenem.

Funding
This study was supported by the:
  • Kerman University of Medical Sciences (Award 96000823 and 98001031)
    • Principle Award Recipient: DavoodKalantar-Neyestanaki
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001361
2021-05-17
2022-01-24
Loading full text...

Full text loading...

References

  1. Ramadan Mohamed E, Ali MY, Waly NGFM, Halby HM, Abd El-Baky RM. The Inc FII plasmid and its contribution in the transmission of blaNDM-1 and blaKPC-2 in Klebsiella pneumoniae in Egypt. Antibiotics 2019; 8:266 [View Article]
    [Google Scholar]
  2. Meatherall BL, Gregson D, Ross T, Pitout JDD, Laupland KB. Incidence, risk factors, and outcomes of Klebsiella pneumoniae bacteremia. Am J Med 2009; 122:866–873 [View Article]
    [Google Scholar]
  3. Dong D, Li M, Liu Z, Feng J, Jia N. Characterization of a NDM-1-encoding plasmid pHFK418-NDM from a clinical Proteus mirabilis strain harboring two novel transposons, Tn6624 and Tn6625. Front Microbiol 2030; 2019:10
    [Google Scholar]
  4. Wang B, Pan F, Wang C, Zhao W, Sun Y et al. Molecular epidemiology of Carbapenem-resistant Klebsiella pneumoniae in a paediatric hospital in China. Int J Infect Dis 2020; 93:311–319 [View Article]
    [Google Scholar]
  5. Ali A, Gupta D, Srivastava G, sharma A, Khan AU. Molecular and computational approaches to understand resistance of New Delhi metallo β-lactamase variants (NDM-1, NDM-4, NDM-5, NDM-6, NDM-7)-producing strains against carbapenems. J Biomol Struct Dyn 2019; 37:2061–2071 [View Article]
    [Google Scholar]
  6. Khan AU, Maryam L, Zarrilli R. Structure, genetics and worldwide spread of new Delhi metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol 2017; 17:101 [View Article][PubMed]
    [Google Scholar]
  7. Liu L, Feng Y, McNally A, Zong Z. Bla NDM-21, a new variant of blaNDM in an Escherichia coli clinical isolate carrying blaCTX-M-55 and rmtB. J Antimicrob Chemother 2018; 73:2336–2339 [View Article]
    [Google Scholar]
  8. Poirel L, Dortet L, Bernabeu S, Nordmann P. Genetic features of blaNDM-1-positive Enterobacterales. Antimicrob Agents Chemother 2011; 55:5403–5407
    [Google Scholar]
  9. Jean SS, Lee WS, Hsueh PR. Ertapenem non-susceptibility and independent predictors of the carbapenemase production among the Enterobacterales strains causing intra-abdominal infections in the Asia-Pacific region: results from the Study for Monitoring Antimicrobial Resistance Trends (SMART). Infect Drug Resist 1881; 2018:11
    [Google Scholar]
  10. Treatment options for colistin resistant Klebsiella pneumoniae: present and future. JCM 2019; 8:934 [View Article]
    [Google Scholar]
  11. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL et al. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 2005; 63:219–228 [View Article]
    [Google Scholar]
  12. Solgi H, Badmasti F, Giske CG, Aghamohammad S, Shahcheraghi F. Molecular epidemiology of NDM-1- and OXA-48-producing Klebsiella pneumoniae in an Iranian Hospital: clonal dissemination of ST11 and ST893. J Antimicrob Chemother 2018; 73:1517–1524 [View Article]
    [Google Scholar]
  13. Hopkins KL, Liebana E, Villa L, Batchelor M, Threlfall EJ et al. Replicon typing of plasmids carrying CTX-M or CMY β-lactamases circulating among Salmonella and Escherichia coli isolates. Antimicrob Agents Chemother 2006; 50:3203–3206 [View Article]
    [Google Scholar]
  14. Carloni E, Andreoni F, Omiccioli E, Villa L, Magnani M et al. Comparative analysis of the standard PCR-based replicon typing (PBRT) with the commercial PBRT-KIT. Plasmid 2017; 90:10–14 [View Article]
    [Google Scholar]
  15. Carattoli A. Plasmids in Gram negatives: molecular typing of resistance plasmids. Int J Med Microbiol 2011; 301:654–658 [View Article]
    [Google Scholar]
  16. Huang TW, Chen TL, Chen YT, Lauderdale TL, Liao TL. Copy number change of the NDM-1 sequence in a multidrug-resistant Klebsiella pneumoniae clinical strain. PLoS One 2013; 29;8:
    [Google Scholar]
  17. Kiaei S, Moradi M, Hosseini-Nave H, Ziasistani M, Kalantar-Neyestanaki D. Endemic dissemination of different sequence types of carbapenem-resistant Klebsiella pneumoniae strains harboring blaNDM and 16S rRNA methylase genes in Kerman hospitals, Iran, from 2015 to 2017. Infect Drug Resist 2019; 12:45
    [Google Scholar]
  18. Qin S, Zhou M, Zhang Q, Tao H, Ye Y et al. First identification of NDM-4-producing Escherichia coli ST410 in China. Emerg Microbes Infect 2016; 5:1–3 [View Article]
    [Google Scholar]
  19. Whelan JA, Russell NB, Whelan MA. A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 2003; 278:261–269 [View Article]
    [Google Scholar]
  20. Wasfi R, Elkhatib WF, Ashour HM. Molecular typing and virulence analysis of multidrug resistant Klebsiella pneumoniae clinical strains recovered from Egyptian hospitals. Sci Rep 2016; 22:6
    [Google Scholar]
  21. Deschaght P, Van Simaey L, Decat E, Van Mechelen E, Brisse S. Rapid genotyping of Achromobacter xylosoxidans, Acinetobacter baumannii, Klebsiella pneumoniae, Pseudomonas aeruginosa and Stenotrophomonas maltophilia strains using melting curve analysis of RAPD-generated DNA fragments (McRAPD). Res Microbiol 2011; 1;162:386–392
    [Google Scholar]
  22. Venieri D, Fraggedaki A, Binas V, Zachopoulos A, Kiriakidis G et al. Study of the generated genetic polymorphisms during the photocatalytic elimination of Klebsiella pneumoniae in water. Photochem Photobiol Sci 2015; 14:506–513 [View Article]
    [Google Scholar]
  23. Surgers L, Boersma P, Girard PM, Homor A, Geneste D. Molecular epidemiology of ESBL-producing E. coli and K. pneumoniae: establishing virulence clusters. Infect Drug Resist 2019; 12:119
    [Google Scholar]
  24. Shintani M, Sanchez ZK, Kimbara K. Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol 2015; 31:242
    [Google Scholar]
  25. Douarre PE, Mallet L, Radomski N, Felten A, Mistou MY. Analysis of COMPASS, a new comprehensive plasmid database revealed prevalence of multireplicon and extensive diversity of IncF plasmids. Front Microbiol 2020; 24:483
    [Google Scholar]
  26. Hancock SJ, Phan M-D, Peters KM, Forde BM, Chong TM et al. Identification of IncA/C plasmid replication and maintenance genes and development of a plasmid multilocus sequence typing scheme. Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  27. Carattoli A, Villa L, Poirel L, Bonnin RA, Nordmann P. Evolution of IncA/C blaCMY-2-carrying plasmids by acquisition of the blaNDM-1 carbapenemase gene. Antimicrob Agents Chemother 2012; 56:783–786
    [Google Scholar]
  28. Arabaghian H, Salloum T, Alousi S, Panossian B, Araj GF et al. Molecular characterization of carbapenem resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae isolated from Lebanon. Sci Rep 2019; 9:1–2 [View Article]
    [Google Scholar]
  29. Bedenić B, Kocsis E, Mazzariol A, Barišić M, Bošnjak Z. Diversity of carbapenemases in clinical strains of Enterobacterales from Croatia; a preliminary results of a multicentre study. 23rd ECCMID; 2013
  30. Carattoli A, García-Fernández A, Varesi P, Fortini D, Gerardi S et al. Molecular epidemiology of Escherichia coli producing extended-spectrum -lactamases isolated in Rome, Italy. J Clin Microbiol 2008; 46:103–108 [View Article]
    [Google Scholar]
  31. Johnson TJ, Nolan LK. Pathogenomics of the virulence plasmids of Escherichia coli. MMBR 2009; 73:750–774 [View Article]
    [Google Scholar]
  32. Sun Q-ling, Gu D, Wang Q, Hu Y, Shu L et al. Dynamic colonization of Klebsiella pneumoniae isolates in gastrointestinal tract of intensive care patients. Front Microbiol 2019; 10:230 [View Article]
    [Google Scholar]
  33. Yang Q-E, Sun J, Li L, Deng H, Liu B-T et al. IncF plasmid diversity in multi-drug resistant Escherichia coli strains from animals in China. Front Microbiol 2015; 6:964 [View Article]
    [Google Scholar]
  34. Villa L, García-Fernández A, Fortini D. Carattoli A. J Antimicrob Chemother 2010; 65:2518–2529
    [Google Scholar]
  35. JJ L, Spychala CN, Hu F, Sheng JF, Doi Y. Complete nucleotide sequences of blaCTX-M-harboring IncF plasmids from community-associated Escherichia coli strains in the United States. Antimicrob Agents Chemother 2015; 59:3002–3007
    [Google Scholar]
  36. Zhang Y, Zhao C, Wang Q, Wang X, Chen 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 [View Article]
    [Google Scholar]
  37. Ali SZ, Ali SM, Khan AU. Prevalence of IncI1-Iγ and IncFIA-FIB type plasmids in extended-spectrum β-lactamase-producing Klebsiella pneumoniae strains isolated from the NICU of a North Indian Hospital. Microbiology 2014; 160:1153–1161 [View Article]
    [Google Scholar]
  38. Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother 2018; 73:1121–1137 [View Article]
    [Google Scholar]
  39. Carattoli A. Resistance plasmid families in Enterobacterales. Antimicrob Agents Chemother 2009; 53:2227–2238 [View Article]
    [Google Scholar]
  40. Adamczuk M, Zaleski P, Dziewit L, Wolinowska R, Nieckarz M. Diversity and global distribution of IncL/M plasmids enabling horizontal dissemination of β-lactam resistance genes among the Enterobacterales. Biomed Res 2015; 2015:
    [Google Scholar]
  41. Carattoli A, Seiffert SN, Schwendener S, Perreten V, Endimiani A. Differentiation of INCL and IncM plasmids associated with the spread of clinically relevant antimicrobial resistance. PLoS One 2015; 10:e0123063 [View Article]
    [Google Scholar]
  42. Markovska R, Schneider I, Ivanova D, Mitov I, Bauernfeind A. Predominance of IncL/M and IncF plasmid types among CTX-M-ESBL-producing Escherichia coli and Klebsiella pneumoniae in Bulgarian hospitals. APMIS 2014; 122:608–615 [View Article]
    [Google Scholar]
  43. Espedido Björn A., Partridge SR, Iredell JR. Bla IMP-4 in different genetic contexts in Enterobacterales isolates from Australia. Antimicrob Agents Chemother 2008; 52:2984–2987 [View Article]
    [Google Scholar]
  44. Zhang C, Feng Y, Liu F, Jiang H, Qu Z et al. A phage-like IncY plasmid carrying the mcr-1 gene in Escherichia coli from a pig farm in China. Antimicrob Agents Chemother 2017; 61:e02035–16 [View Article]
    [Google Scholar]
  45. Johnson TJ, Wannemuehler YM, Johnson SJ, Logue CM, White DG. Plasmid replicon typing of commensal and pathogenic Escherichia coli strains. Appl Environ Microbiol 2007; 73:
    [Google Scholar]
  46. Bahl MI, Burmølle M, Meisner A, Hansen LH, Sørensen SJ. All IncP-1 plasmid subgroups, including the novel ε subgroup, are prevalent in the influent of a Danish wastewater treatment plant. Plasmid 2009; 62:134–139 [View Article]
    [Google Scholar]
  47. Norberg P, Bergström M, Jethava V, Dubhashi D, Hermansson M. The IncP-1 plasmid backbone adapts to different host bacterial species and evolves through homologous recombination. Nat Commun 2011; 2:1 [View Article][PubMed]
    [Google Scholar]
  48. SS M, Telke AA, Osei KO, Sekse C, Slettemeås JS. blaCTX–M–1/IncI1-Iγ Plasmids Circulating in Escherichia coli From Norwegian Broiler Production are Related, but Distinguishable. Front Microbiol 2020; 5:333
    [Google Scholar]
  49. Johnson TJ, Shepard SM, Rivet B, Danzeisen JL, Carattoli A. Comparative genomics and phylogeny of the IncI1 plasmids: a common plasmid type among porcine enterotoxigenic Escherichia coli. Plasmid 2011; 66:144–151 [View Article]
    [Google Scholar]
  50. Bortolaia V, Guardabassi L, Trevisani M, Bisgaard M, Venturi L et al. High diversity of extended-spectrum β-lactamases in Escherichia coli isolates from Italian broiler flocks. Antimicrob Agents Chemother 2010; 54:1623–1626 [View Article]
    [Google Scholar]
  51. Kakuta N, Nakano R, Nakano A, Suzuki Y, Masui T et al. Molecular characteristics of extended-spectrum β-lactamase-producing Klebsiella pneumoniae in Japan: Predominance of CTX-M-15 and emergence of hypervirulent clones. Int J Infect Dis 2020; 98:281–286 [View Article]
    [Google Scholar]
  52. Hashemizadeh Z, Mansouri S, Pahlavanzadeh F, Morones-Ramírez JR, Tabatabaeifar F. Evaluation of chromosomally and acquired mechanisms of resistance to carbapenem antibiotics among clinical isolates of Pseudomonas aeruginosa in Kerman, Iran. Gene Rep 2021; 100918:
    [Google Scholar]
  53. Wailan AM, Paterson DL. The spread and acquisition of NDM-1: a multifactorial problem. Expert Rev Anti Infect Ther 2014; 12:91–115 [View Article]
    [Google Scholar]
  54. Sartor AL, Raza MW, Abbasi SA, Day KM, Perry JD et al. Molecular epidemiology of NDM-1-producing Enterobacterales and Acinetobacter baumannii isolates from Pakistan. Antimicrob Agents Chemother 2014; 58:5589–5593 [View Article]
    [Google Scholar]
  55. Sonnevend A, Al Baloushi A, Ghazawi A, Hashmey R, Girgis S et al. Emergence and spread of NDM-1 producer Enterobacteriaceae with contribution of IncX3 plasmids in the United Arab Emirates. J Med Microbiol 2013; 62:1044–1050 [View Article]
    [Google Scholar]
  56. Gokmen TG, Togrul Nagiyev MM, Onlen C, Heydari F, Koksal F. NDM-1 and rmtC-producing Klebsiella pneumoniae strains in Turkey. Jundishapur J Microbiol 2016; 9:
    [Google Scholar]
  57. Jamal WY, Albert MJ, Rotimi VO. High prevalence of new Delhi metallo-β-lactamase-1 (NDM-1) producers among carbapenem-resistant EnterobacteralesEnterobacteriaceae in Kuwait. PLoS One 2016; 11:e0152638 [View Article]
    [Google Scholar]
  58. Blanc DS. The use of molecular typing for epidemiological surveillance and investigation of endemic nosocomial infections. Infect Genet Evol 2004; 4:193–197 [View Article]
    [Google Scholar]
  59. Kong H-K, Liu X, Lo WU, Pan Q, Law COK et al. Identification of plasmid-encoded sRNAs in a blaNDM-1-Harboring multidrug-resistance plasmid pNDM-HK in EnterobacteralesEnterobacteriaceae. Front Microbiol 2018; 9:532 [View Article]
    [Google Scholar]
  60. Paul D, Bhattacharjee A, Bhattacharjee D, Dhar D, Maurya AP et al. Transcriptional analysis of bla NDM-1 and copy number alteration under carbapenem stress. Antimicrob Resist Infect Control 2017; 6:26 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001361
Loading
/content/journal/jmm/10.1099/jmm.0.001361
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error