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Spreading of NDMI-Producing Klebsiella Pneumoniaein Different Wards at Assiut University Hospital

Eman Ramadan Mohamed , Hamada Mohamed Halby, Mamdouh Yones Ali, Rehab Mahmoud Abd El-Baky, Nancy G F M Waly
American Journal of Infectious Diseases and Microbiology. 2020, 8(1), 24-28. DOI: 10.12691/ajidm-8-1-4
Received December 26, 2019; Revised February 05, 2020; Accepted February 22, 2020

Abstract

Spreading of NDMI-producing klebsiella pneumoniaehas become a great trouble in many Egyptian hospitalized patients. Localizing the source of these isolates is an important step to prevent their spread in this country. This study included 33 NDMI-producing klebsiella pneumoniae that collected from different clinical specimens of patients admitted to different wards at Assiut University Hospitals in Egypt and confirmed to produce blaNDM1 gene by polymerase chain reaction. Isolates were typed by Enterobacterial Repetitive Intergenic Consensus (ERIC). Respiratory samples (51%) were the predominant samples and chestdepartment was the major ward (48.48%) that isolates recovered. ERIC gel profile showed that several identical isolates were found especially in chest ward and between different medical wards of this hospital suggested clonal transmission of NDMI-producing K. pneumoniae. Also, there are differences in the number and size of ERIC-PCR profiles indicated the genetic diversity among NDMI-producing K. pneumoniae isolates. The results of this study may help in tracing and controlling NDM-1-producing K. pneumoniae outbreak by applying effective infection control measures especially in the chest ward of this hospital.

1. Introduction

K. pneumoniaehas become a great challenge for infection control in human health that can cause life-threatening several infections, such as blood stream infection, pneumonia, urinary tract, post-surgical, and intensive care-related infections 1. Such infections result in increasing morbidity, mortality and medical hospital costs 2.

K. pneumoniae can resist carbapenem drugs by numerousmechanisms, Production of carbapenemases is the most mechanism 3. New Delhi-metallo beta-lactamase (NDM) is the most importantnovel metallo-beta-lactamase that can hydrolyze to nearly all β-lactams 3, 4.It was firstly reported in aSwedish patient traveled to New Delhi 5. Then, worldwide spread of NDM-1-producing isolates have also reported 6. However, NDM1-producing K. pneumoniaeis emerged in numerous Egyptian hospital 7, 8, 9 study on dissemination mechanism of blaNDM1 gene by clonal similarityis limited.

Typing for distinguishing bacterial isolates of the same species are essential epidemiological tools in tracing the source of infection 10. Enterobacterial Repetitive Intergenic Consensus (ERIC) is considered molecular typing tool used in determining the clonal transfer of K. pneumoniae infection in many hospital settings 11, 12. This study is performed to help in tracing and stopping dissemination of NDM1-producing K. pneumoniaein our hospital.

2. Material and Methods

2.1. Study Design

This study is a hospital based observational study, conducted for a period of 14 months from April 2018 to May 2019 on 126 Klebsiella pneumoniae isolates obtained from different clinical specimens of 126 patients admitted to different wards at Assiut University Hospital in Egypt.

2.2. Sample Collection

Samples were collected in a sterile container from each patient according to sites of infections.; they included blood, peritoneal fluid, urine, respiratory secretions, wound swabs, and cerebrospinal fluid. Only one isolate per patient was included. They were transported to Infection Control Lab. within 2 hours of collection. Viable bacterial count was done for urine samples 13 and blood culture was done for blood samples 14. Quantitative culture of endotracheal aspirate (EA) 15.

2.3. Isolation and Identification of K. Pneumoniae

Bacterial identification to the species level were carried out by colonial morphology on MacConkey's agar plates (oxoid, UK), Gram stained films, biochemical reactions including oxidase, motility, indole, methyl red, voges-proskauer, citrate and urease tests and confirmed with API 20E (BioMerieux, Inc., Hazelwood, MO).

2.4. DNA Isolation

Klebsiella isolates were cultured in Luria-Broth medium (Oxoid, Hampshire, England) overnight at 37 °C. DNA isolation of each isolate was done using Genomic Purification Kit (Fermentas, Lithuania) based on the manufacturer's protocol.

2.5 Detection of Carbapenem Resistant K. Pneumoniae

Modified carbapenem inactivation methods (mCIM) were performed as described by byPierce et al 16 for Suspected Carbapenemase-Producing K. pneumoniae isolates. EDTA-modified carbapenem inactivation method (eCIM) for detection of MβL enzymes 17.

2.6. Detection of Bla NDM1 Gene

The genebla NDM-1 was amplified using primers and conditions as described by 18. The sequences of primers used is F (GGTTTGGCGATCTGGTTTTC-3´) and R(CGGAATGGCTCATCACGATC-3´). A volume of 2μL of template DNA was added to a final volume of 25 μL PCR mixture comprising 12.5 μL of Taq PCR Master Mix (Fermentas, UK), including, 1× PCR buffer, 1.5 mmol/L MgCl2, 0.15 mmol/L dNTP, and 1.25 IU Taq DNA polymerase, 1 μL of 0.8 μmol/L each primer and 9.5 μL of sterile distilled water. The amplicon size was 621 bp and was analyzed by electrophoresis in a 1.5% agarose gel.

2.7. ERIC-PCR

ERIC-PCR was applied using the primers, ERIC1 (5′-ATGTAAGCTCCTGGGGATTCAC-3′) and ERIC2 (5′-AAGTAAGTGACTGGGGTGAGCG-3′) for K. pneumoniae isolates 19. PCRAmplifications were performed in a 25 μL solution under the following conditions: an initial denaturation at 94°C for 5 min; 1 min at 94°C, 1 min at 39°C, and 5 min at 72°C; and a final extension at 72°C for 10 min.Denaturation, annealing, and extension were performed in 35 cycles. ERIC-PCR products were detected by a 2.0% agarose gel electrophoresis, and the gel was visualized with UV. Products sizes were estimated using 100 bp and 1 kb DNA ladders (New England Biolabs) as molecular size markers.

2.8. DNA Fingerprinting

Analyses of the DNA fingerprints were presented by BioNumerics software version 7.6 (Applied Maths, Belgium). A cutoff value similarity was applied to define identical strains as closely related isolates with ≥95% similarity and isolates with <95% similarity as unrelated strains. The similarity between the profiles was evaluated with the band matching Dice coefficient, and dendrogramwas produced by the unweighted pair group method with arithmetic averages (UPGMA).

3. Results

3.1. Identification of K. Pneumoniae Isolates

K. pneumoniae which identified by conventional biochemical tests was confirmed and fully investigated by using the API 20E system. The API20E Index system identified Klebsiella Pneumoniae with two different analytical profile index numbers with 5215773 code and 1215773 code.

3.2. Patients and Isolates Characteristics

One hundred and twenty-six Klebsiella pneumoniae strains isolated from different departments at Assiut University Hospital (April 2018 to May 2019) were tested for carbapenemase enzymes production using mCIM and eCIM.Carbapenemase activity was found in 77/126 (61.1%) of the K. pneumoniae isolates. BlaNDM1 was positive in 43/77 (55.84%) isolates.

This study included 33 patientsout of 43 with confirmed NDMI-producing K. pneumoniaeinfections. The isolates were obtained from 19 male and 14 female patients. Patients were generally elderly (median age was 50 years, with a range of 40–63 years. Respiratory samples (51%) were the predominant sourcesof KP, followed by urine (21%), wound (16%), blood (6%), and catheter tip (6%) samples.

3.3. The Different Medical Wards from which the 33 NDMI-Producing Isolates were Recovered

Mostly of Medical Wards from which the clinical Klebsiella isolates recovered were Chest Department (48.48%) and Gastrointestinal tract wards (18.18%) as presented in Table 1.

3.4. Production of Bla NDMI Gene

K. pneumoniae isolates were confirmed to produce NDMI gene by PCR method. Amplicon size was 621bp as appeared in Figure 1.

3.5. ERIC profiles of NDMI-Producing K. Pneumoniae

All 33 NDMI-producing K. pneumoniaeisolates were genotyped by ERIC that showed greater genetic diversity of the isolates (Figure 2). The electrophoretic analysis of the PCR reaction products has revealed that the number of bands ranged from 1 to 5. The sizes of the PCR products ranged from 100 bp to more than 1000 bp.

3.6. DNA Fingerprinting

By analyzing the ERIC-PCR profiles, the 33 isolates were categorized into 25 ERIC-types. Isolates sharing greater or equal to 95% of the bands were classified in the same clusters as presented in the dendrogram (Figure 3). ERIC identified fifteen (15) types of K. pneumoniae that were designated as follows: type A (n=4), type B (n=3) and two isolates in each type from C to type E. The remaining unrelated (n=20) isolates with <95% similarity that belonged to types F1 to F 20 had one isolates in each type as shown in Table 2.

4. Discussion

K. pneumoniae is known as the main organisms that cause nosocomial infections including bacteremia, pneumonia, urinary tract infections, intra-abdominal infections, sepsis and gastroenteritis especially in developing countries 1, 2. It can easily acquire antibiotic resistant causing a global challenge to human health 20. carbapenem resistant K. pneumoniaehas become more problem in limiting of treatment option 21, 22. It can produce blaNDMI gene to hydrolyze carbapenem drugs 23. There was a spread of carbapenem resistant K. pneumoniae in many hospitals of our regionduring the last few years 7, 8, 9. Additionally, it was approvedpreviously that different clones of K. pneumoniaecan spread easily in one ward (PICU) of this hospital 24. As a result, a need for localizing the source and controlling the spread of NDM1-producing K. pneumoniaein different wards within this hospital should be employed. PCR-based ERIC fingerprinting isa quick method useful for typing the strains of K. Pneumoniae 11.

In this study, Respiratory samples (51%) were the predominant samples and Chest Department was the major ward (48.48%) that isolates recovered. This may be the airway is the most common presentations of K. pneumoniae in hospitals 25.

By imagining of the ERIC gel profiles, several identical isolates were found suggested clonal transmission of K. pneumoniae in different medical wards of this hospital 26. Also, there are differences in the number and size of ERIC-PCR profiles indicated the genetic diversity among NDMI-producing K. pneumoniaeisolates.

In this study, mostof ERIC profiles exhibited in type A (S8, S9, S11, S13). This clone spread dramatically in chest ward that proved K. pneumoniae can spread easily by respiratory droplet. Additionally, this clone appeared (S11) in neurology department that may indicate transfer of blaNDMI gene to another ward by this clone. Another clone (type C) can spread between two patients in chest ward presented in isolates 3 and 10.

ERICshowed that three of NDMI-producing K. pneumoniae isolates (S28,S29, S31) from injury, chest and GIT departments belonged to the same cluster (type B) which suggested that this clone that harbor NDM1 can spread between patients in different wardsindicating that easily spread of hospital acquired NDMI-producingK. pneumoniae.

Similar strains were detected between two isolates (S18, S19) from general reception and chest (type D) and similarity was also detected (type E) between 2 isolates (S21, S22) from surgery and chest wards, demonstrated that chest ward could be the common factor of spread of the carbapenem resistant of K. pneumoniaeto other wards of this hospital and may be the origin of spreading 27.

However, genetic analysis using ERIC-PCR showed that majority of NDMI-producing isolates(n=20) were clonally unrelated, suggesting that dissemination of NDMI genemay due to possible horizontal transmission between non similar patterns by conjugative plasmid 28, 29.

The results of this study represent a need to additional precaution to rationalize carbapenem drugs, develop hygiene measures and effective infection control measures to control this NDM-1-producing K. pneumoniae outbreak especially in the chest ward of this hospital.

5. Conclusion

Highly resistant of NDMI- producing K. pneumoniae should be traced and controlled especially in developing country. More typing methods are needed for estimation of the genetic relatedness and tracing the sources of infection to other hospitals by this pathogen.

Acknowledgements

The authors are thankful to Professor Dr. Asmaa Omar Ahmed and the infection control team, as well as the nurses and health-care workers at the Assiut University Hospital, for their assistance throughout the course of the study.

Conflict of Interest

The authors have no competing interests.

References

[1]  Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit J-C, Offenstadt G, et al. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. Journal of clinical microbiology. 2011; 49: 3012-4.
In article      View Article  PubMed
 
[2]  Foglia E, Meier MD, Elward A. Ventilator-associated pneumonia in neonatal and pediatric intensive care unit patients. Clinical microbiology reviews. 2007;20:409-25.
In article      View Article  PubMed
 
[3]  Yan J, Pu S, Jia X, Xu X, Yang S, Shi J, et al. Multidrug resistance mechanisms of carbapenem resistant Klebsiella pneumoniae strains isolated in Chongqing, China. Annals of laboratory medicine. 2017; 37: 398-407.
In article      View Article  PubMed
 
[4]  Miriagou V, Cornaglia G, Edelstein M, Galani I, Giske C, Gniadkowski M, et al. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clinical microbiology and infection. 2010; 16: 112-22.
In article      View Article  PubMed
 
[5]  Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-lactamase gene, bla NDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrobial agents and chemotherapy. 2009; 53: 5046-54.
In article      View Article  PubMed
 
[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 microbiology. 2017; 17: 101.
In article      View Article  PubMed
 
[7]  El-Sweify M, Gomaa N, El-Maraghy N, Mohamed H. Phenotypic Detection of Carbapenem Resistance among Klebsiella pneumoniae in Suez Canal University Hospitals, Ismailiya, Egypt. International Journal of Current Microbiology and Applied Sciences. 2015; 4: 10-8.
In article      
 
[8]  Gamal D, Fernández-Martínez M, Salem D, El-Defrawy I, Montes LÁ, Ocampo-Sosa AA, et al. Carbapenem-resistant Klebsiella pneumoniae isolates from Egypt containing blaNDM-1 on IncR plasmids and its association with rmtF. International Journal of Infectious Diseases. 2016; 43: 17-20.
In article      View Article  PubMed
 
[9]  Morsi SS. Comparative Evaluation of Phenotypic and Genotypic Methods for Detection of Carbapenemases in Clinically Significant Klebsiella pneumoniae Isolates. The Egyptian Journal of Medical Microbiology. 2016; 38: 1-8.
In article      View Article
 
[10]  Christian NA, Roye-Green K, Smikle M. Molecular epidemiology of multidrug resistant extended spectrum beta-lactamase producing Klebsiella pneumoniae at a Jamaican hospital, 2000-2004. BMC microbiology. 2010; 10: 27.
In article      View Article  PubMed
 
[11]  Seifi K, Kazemian H, Heidari H, Rezagholizadeh F, Saee Y, Shirvani F, et al. Evaluation of biofilm formation among Klebsiella pneumoniae isolates and molecular characterization by ERIC-PCR. Jundishapur journal of microbiology. 2016; 9.
In article      View Article  PubMed
 
[12]  Zhang S, Yang G, Ye Q, Wu Q, Zhang J, Huang Y. Phenotypic and genotypic characterization of Klebsiella pneumoniae isolated from retail foods in China. Frontiers in microbiology. 2018; 9: 289.
In article      View Article  PubMed
 
[13]  Hedges A. Estimating the precision of serial dilutions and viable bacterial counts. International journal of food microbiology. 2002; 76: 207-14.
In article      View Article
 
[14]  Madeo M, Barlow G. Reducing blood-culture contamination rates by the use of a 2% chlorhexidine solution applicator in acute admission units. Journal of Hospital Infection. 2008; 69: 307-9.
In article      View Article  PubMed
 
[15]  Shin YM, Oh Y-M, Kim MN, Shim TS, Lim C-M, Lee SD, et al. Usefulness of quantitative endotracheal aspirate cultures in intensive care unit patients with suspected pneumonia. Journal of Korean medical science. 2011; 26: 865-9.
In article      View Article  PubMed
 
[16]  Pierce VM, Simner PJ, Lonsway DR, Roe-Carpenter DE, Johnson JK, Brasso WB, et al. Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among Enterobacteriaceae. Journal of clinical microbiology. 2017; 55: 2321-33.
In article      View Article  PubMed
 
[17]  Sfeir M, Hayden J, Fauntleroy K, Mazur C, Johnson J, Simner P, et al. EDTA-modified carbapenem inactivation method: a phenotypic method for detecting metallo-β-lactamase-producing Enterobacteriaceae. Journal of clinical microbiology. 2019; 57: e01757-18.
In article      View Article  PubMed
 
[18]  Poirel L, Dortet L, Bernabeu S, Nordmann P. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrobial agents and chemotherapy. 2011; 55: 5403-7.
In article      View Article  PubMed
 
[19]  Versalovic J, Koeuth T, Lupski R. Distribution of repetitive DNA sequences in eubacteria and application to finerpriting of bacterial enomes. Nucleic acids research. 1991; 19: 6823-31.
In article      View Article  PubMed
 
[20]  Pitout JD, Nordmann P, Poirel L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrobial agents and chemotherapy. 2015; 59: 5873-84.
In article      View Article  PubMed
 
[21]  Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerging infectious diseases. 2011; 17: 1791.
In article      View Article  PubMed
 
[22]  Patel G, Huprikar S, Factor SH, Jenkins SG, Calfee DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infection Control & Hospital Epidemiology. 2008; 29: 1099-106.
In article      View Article  PubMed
 
[23]  Nordmann P, Poirel L, Walsh TR, Livermore DM. The emerging NDM carbapenemases. Trends in microbiology. 2011; 19: 588-95.
In article      View Article  PubMed
 
[24]  Mohamed ER, Aly SA, Halby HM, Ahmed SH, Zakaria AM, El-Asheer OM. Epidemiological typing of multidrug-resistant Klebsiella pneumoniae, which causes paediatric ventilator-associated pneumonia in Egypt. Journal of medical microbiology. 2017; 66: 628-34.
In article      View Article  PubMed
 
[25]  Sydnor ER, Perl TM. Hospital epidemiology and infection control in acute-care settings. Clinical microbiology reviews. 2011; 24: 141-73.
In article      View Article  PubMed
 
[26]  Wang X, Chen G, Wu X, Wang L, Cai J, Chan EW, et al. Increased prevalence of carbapenem resistant Enterobacteriaceae in hospital setting due to cross-species transmission of the blaNDM-1 element and clonal spread of progenitor resistant strains. Frontiers in microbiology. 2015; 6: 595.
In article      View Article  PubMed
 
[27]  Yu F, Ying Q, Chen C, Li T, Ding B, Liu Y, et al. Outbreak of pulmonary infection caused by Klebsiella pneumoniae isolates harbouring blaIMP-4 and blaDHA-1 in a neonatal intensive care unit in China. Journal of medical microbiology. 2012; 61: 984-9.
In article      View Article  PubMed
 
[28]  Huang X, Cheng X, Sun P, Tang C, Ni F, Liu G. Characteristics of NDM-1-producing Klebsiella pneumoniae ST234 and ST1412 isolates spread in a neonatal unit. BMC microbiology. 2018; 18: 186.
In article      View Article  PubMed
 
[29]  Ramadan Mohamed E, Ali MY, Waly NG, 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.
In article      View Article  PubMed
 

Published with license by Science and Education Publishing, Copyright © 2020 Eman Ramadan Mohamed, Hamada Mohamed Halby, Mamdouh Yones Ali, Rehab Mahmoud Abd El-Baky and Nancy G F M Waly

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Cite this article:

Normal Style
Eman Ramadan Mohamed, Hamada Mohamed Halby, Mamdouh Yones Ali, Rehab Mahmoud Abd El-Baky, Nancy G F M Waly. Spreading of NDMI-Producing Klebsiella Pneumoniaein Different Wards at Assiut University Hospital. American Journal of Infectious Diseases and Microbiology. Vol. 8, No. 1, 2020, pp 24-28. http://pubs.sciepub.com/ajidm/8/1/4
MLA Style
Mohamed, Eman Ramadan, et al. "Spreading of NDMI-Producing Klebsiella Pneumoniaein Different Wards at Assiut University Hospital." American Journal of Infectious Diseases and Microbiology 8.1 (2020): 24-28.
APA Style
Mohamed, E. R. , Halby, H. M. , Ali, M. Y. , El-Baky, R. M. A. , & Waly, N. G. F. M. (2020). Spreading of NDMI-Producing Klebsiella Pneumoniaein Different Wards at Assiut University Hospital. American Journal of Infectious Diseases and Microbiology, 8(1), 24-28.
Chicago Style
Mohamed, Eman Ramadan, Hamada Mohamed Halby, Mamdouh Yones Ali, Rehab Mahmoud Abd El-Baky, and Nancy G F M Waly. "Spreading of NDMI-Producing Klebsiella Pneumoniaein Different Wards at Assiut University Hospital." American Journal of Infectious Diseases and Microbiology 8, no. 1 (2020): 24-28.
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  • Figure 1. Gel electrophoresis of the PCR-amplified products for detection of blaNDM1. Lane M is DNA marker (100-1500bp); lane 1 is a positive control, lanes 2,3,4,6,8 are positive samples (621 bp) and lane 5,7 are negative samples for blaNDM1
[1]  Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit J-C, Offenstadt G, et al. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. Journal of clinical microbiology. 2011; 49: 3012-4.
In article      View Article  PubMed
 
[2]  Foglia E, Meier MD, Elward A. Ventilator-associated pneumonia in neonatal and pediatric intensive care unit patients. Clinical microbiology reviews. 2007;20:409-25.
In article      View Article  PubMed
 
[3]  Yan J, Pu S, Jia X, Xu X, Yang S, Shi J, et al. Multidrug resistance mechanisms of carbapenem resistant Klebsiella pneumoniae strains isolated in Chongqing, China. Annals of laboratory medicine. 2017; 37: 398-407.
In article      View Article  PubMed
 
[4]  Miriagou V, Cornaglia G, Edelstein M, Galani I, Giske C, Gniadkowski M, et al. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clinical microbiology and infection. 2010; 16: 112-22.
In article      View Article  PubMed
 
[5]  Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-lactamase gene, bla NDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrobial agents and chemotherapy. 2009; 53: 5046-54.
In article      View Article  PubMed
 
[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 microbiology. 2017; 17: 101.
In article      View Article  PubMed
 
[7]  El-Sweify M, Gomaa N, El-Maraghy N, Mohamed H. Phenotypic Detection of Carbapenem Resistance among Klebsiella pneumoniae in Suez Canal University Hospitals, Ismailiya, Egypt. International Journal of Current Microbiology and Applied Sciences. 2015; 4: 10-8.
In article      
 
[8]  Gamal D, Fernández-Martínez M, Salem D, El-Defrawy I, Montes LÁ, Ocampo-Sosa AA, et al. Carbapenem-resistant Klebsiella pneumoniae isolates from Egypt containing blaNDM-1 on IncR plasmids and its association with rmtF. International Journal of Infectious Diseases. 2016; 43: 17-20.
In article      View Article  PubMed
 
[9]  Morsi SS. Comparative Evaluation of Phenotypic and Genotypic Methods for Detection of Carbapenemases in Clinically Significant Klebsiella pneumoniae Isolates. The Egyptian Journal of Medical Microbiology. 2016; 38: 1-8.
In article      View Article
 
[10]  Christian NA, Roye-Green K, Smikle M. Molecular epidemiology of multidrug resistant extended spectrum beta-lactamase producing Klebsiella pneumoniae at a Jamaican hospital, 2000-2004. BMC microbiology. 2010; 10: 27.
In article      View Article  PubMed
 
[11]  Seifi K, Kazemian H, Heidari H, Rezagholizadeh F, Saee Y, Shirvani F, et al. Evaluation of biofilm formation among Klebsiella pneumoniae isolates and molecular characterization by ERIC-PCR. Jundishapur journal of microbiology. 2016; 9.
In article      View Article  PubMed
 
[12]  Zhang S, Yang G, Ye Q, Wu Q, Zhang J, Huang Y. Phenotypic and genotypic characterization of Klebsiella pneumoniae isolated from retail foods in China. Frontiers in microbiology. 2018; 9: 289.
In article      View Article  PubMed
 
[13]  Hedges A. Estimating the precision of serial dilutions and viable bacterial counts. International journal of food microbiology. 2002; 76: 207-14.
In article      View Article
 
[14]  Madeo M, Barlow G. Reducing blood-culture contamination rates by the use of a 2% chlorhexidine solution applicator in acute admission units. Journal of Hospital Infection. 2008; 69: 307-9.
In article      View Article  PubMed
 
[15]  Shin YM, Oh Y-M, Kim MN, Shim TS, Lim C-M, Lee SD, et al. Usefulness of quantitative endotracheal aspirate cultures in intensive care unit patients with suspected pneumonia. Journal of Korean medical science. 2011; 26: 865-9.
In article      View Article  PubMed
 
[16]  Pierce VM, Simner PJ, Lonsway DR, Roe-Carpenter DE, Johnson JK, Brasso WB, et al. Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among Enterobacteriaceae. Journal of clinical microbiology. 2017; 55: 2321-33.
In article      View Article  PubMed
 
[17]  Sfeir M, Hayden J, Fauntleroy K, Mazur C, Johnson J, Simner P, et al. EDTA-modified carbapenem inactivation method: a phenotypic method for detecting metallo-β-lactamase-producing Enterobacteriaceae. Journal of clinical microbiology. 2019; 57: e01757-18.
In article      View Article  PubMed
 
[18]  Poirel L, Dortet L, Bernabeu S, Nordmann P. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrobial agents and chemotherapy. 2011; 55: 5403-7.
In article      View Article  PubMed
 
[19]  Versalovic J, Koeuth T, Lupski R. Distribution of repetitive DNA sequences in eubacteria and application to finerpriting of bacterial enomes. Nucleic acids research. 1991; 19: 6823-31.
In article      View Article  PubMed
 
[20]  Pitout JD, Nordmann P, Poirel L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrobial agents and chemotherapy. 2015; 59: 5873-84.
In article      View Article  PubMed
 
[21]  Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerging infectious diseases. 2011; 17: 1791.
In article      View Article  PubMed
 
[22]  Patel G, Huprikar S, Factor SH, Jenkins SG, Calfee DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infection Control & Hospital Epidemiology. 2008; 29: 1099-106.
In article      View Article  PubMed
 
[23]  Nordmann P, Poirel L, Walsh TR, Livermore DM. The emerging NDM carbapenemases. Trends in microbiology. 2011; 19: 588-95.
In article      View Article  PubMed
 
[24]  Mohamed ER, Aly SA, Halby HM, Ahmed SH, Zakaria AM, El-Asheer OM. Epidemiological typing of multidrug-resistant Klebsiella pneumoniae, which causes paediatric ventilator-associated pneumonia in Egypt. Journal of medical microbiology. 2017; 66: 628-34.
In article      View Article  PubMed
 
[25]  Sydnor ER, Perl TM. Hospital epidemiology and infection control in acute-care settings. Clinical microbiology reviews. 2011; 24: 141-73.
In article      View Article  PubMed
 
[26]  Wang X, Chen G, Wu X, Wang L, Cai J, Chan EW, et al. Increased prevalence of carbapenem resistant Enterobacteriaceae in hospital setting due to cross-species transmission of the blaNDM-1 element and clonal spread of progenitor resistant strains. Frontiers in microbiology. 2015; 6: 595.
In article      View Article  PubMed
 
[27]  Yu F, Ying Q, Chen C, Li T, Ding B, Liu Y, et al. Outbreak of pulmonary infection caused by Klebsiella pneumoniae isolates harbouring blaIMP-4 and blaDHA-1 in a neonatal intensive care unit in China. Journal of medical microbiology. 2012; 61: 984-9.
In article      View Article  PubMed
 
[28]  Huang X, Cheng X, Sun P, Tang C, Ni F, Liu G. Characteristics of NDM-1-producing Klebsiella pneumoniae ST234 and ST1412 isolates spread in a neonatal unit. BMC microbiology. 2018; 18: 186.
In article      View Article  PubMed
 
[29]  Ramadan Mohamed E, Ali MY, Waly NG, 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.
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