American Journal of Internal Medicine
Volume 5, Issue 1, January 2017, Pages: 1-6

Emergence of Gram-Negative Bacilli with Concomitant blaNDM-1- and blaOXA-48-Like Genes in Egypt

Maha Assem1, Mohamed-Naguib Abdalla Wifi1, Rasha Elsherif2, Ahmed Saad1,
Dalia Kadry Ismail2, Ahmed Hasanin3, Rasha Bassyouni4, Mohamed Saeed Hussein Gomaa1

1Internal Medicine Department, Faculty of Medicine, Cairo University, Cairo, Egypt

2Clinical and Chemical Pathology Department, Faculty of Medicine, Cairo University, Cairo, Egypt

3Anesthesiology Department, Faculty of Medicine, Cairo University, Cairo, Egypt

4Medical Microbiology and Immunology Department, Faculty of Medicine, Fayoum University, Fayoum, Egypt

Email address:

(M. Assem)
(Mohamed-Naguib A. W.)
(Mohamed-Naguib A. W.)
(R. Elsherif)
(A. Saad)
(D. K. Ismail)
(A. Hasanin)
(R. Bassyouni)
(M. S. H. Gomaa)

To cite this article:

Maha Assem, Mohamed-Naguib Abdalla Wifi, Rasha Elsherif, Ahmed Saad, Dalia Kadry Ismail, Ahmed Hasanin, Rasha Bassyouni, Mohamed Saeed Hussein Gomaa. Emergence of Gram-Negative Bacilli with Concomitant blaNDM-1- and blaOXA-48-Like Genes in Egypt. American Journal of Internal Medicine. Vol. 5, No. 1, 2017, pp. 1-6. doi: 10.11648/j.ajim.20170501.11

Received: November 15, 2016; Accepted: November 30, 2016; Published: January 3, 2017

Abstract: Multidrug-resistant Gram-negative organisms have emerged as a major threat to hospitalized patients, and are associated with serious morbidity and mortality. This study aimed to characterize carbapenem resistance genes among Gram-negative bacilli isolated from clinical samples from patients in the intensive care unit of Cairo University Hospital. A total of 211 samples were collected from patients showing clinical evidence of infection. Bacteria were isolated and identified by conventional microbiological methods. Acinetobacter baumannii isolates were furtherly characterized by polymerase chain reaction (PCR), using primers specific for blaOXA-51-like genes. The Kirby Bauer disc diffusion method was used to determine susceptibility patterns of isolates, and carbapenem resistance was further examined by a modified Hodge test. Positive isolates were tested for the presence of blaKPC, blaOXA-48, and blaNDM-like genes by PCR. NDM gene types were determined by direct sequencing. From the 211 samples, 229 Gram-negative bacilli were isolated. Fifty isolates (21.2%) were resistant to carbapenem. PCR analysis showed that none of the 50 isolates carried blaKPC-like genes, while 24 (48%) isolates carried blaOXA-48-like genes, 8 (16%) carried blaNDM-1, and five isolates (10%) carried both blaNDM-1 and blaOXA-48-like genes. These results indicate that continuous surveillance of these multidrug-resistant pathogens is urgently required. And that is very important is to activate the antimicrobial stewardship programs of which the most important is restriction of the big gun antibiotics like carbapenems, colistin, tigecyclin and vancomycin and restricting their prescription to privileged specialties.

Keywords: Carbapenem Resistance, Gram-negative Bacilli, blaOXA-48, blaNDM-1

1. Introduction

"Infections caused by Gram-negative bacilli (GNB) are of particular concern, especially in intensive care units (ICUs). These organisms are highly efficient at acquiring or up-regulating genes that code for mechanisms of antibiotic resistance, especially in the presence of antibiotic selection pressure. Furthermore, they contain a variety of resistance pathways, and often contain multiple mechanisms targeting the same antibiotic [1]". "Gram-negative bacteria resistant to three or more antimicrobial classes, known as Multidrug-resistant (MDR) Gram-negative organisms, have emerged as a major threat to hospitalized patients and have been associated with mortality rates ranging from 30–70% [2], [3]". "A range of Gram-negative organisms, including both non-fermenters (Acinetobacter baumannii and Pseudomonas aeruginosa) and fermenters (Enterobacteriaecae), are responsible for hospital-acquired infections. MDR organisms, including A. baumannii, P. aeruginosa, and extended-spectrum β-lactamase-producing or carbapenemase-producing Enterobacteriaceae, are increasingly being reported worldwide [1]".

"Among the Enterobacteriaceae, the most clinically significant carbapenemases belong to the Ambler molecular class A (Klebsiella pneumoniae carbapenemase, KPC), class B (Verona-Integron Mediated, VIM; instance plasmid-mediated IMP; and New Delhi metallo-β-lactamases, NDM), and class D expanded-spectrum oxacillinase (OXA-23 and OXA-48) types [4]"."Recently, NDM-type enzymes have been identified among Enterobacteriaceae in Egypt. Like KPCs, these enzymes are frequently found on mobile genetic elements and have the potential to become widespread [5]".

"Patients in the ICU usually have serious co-morbid conditions or are compromised by invasive procedures, such as mechanical ventilation, surgery, and frequent use of vascular or urinary catheters. Infections in these patients are usually life threatening and may be caused by MDR organisms [6]". "Carbapenem antibiotics have traditionally been considered the last line of defense in treating infections caused by these bacteria but nowadays we have colistin (polymexin E) is last line of defense against MDR gram negative bacteria. [7]" "Recently Qureshi et al. reported Colistin-resistant A. baumannii almost exclusively among patients who had received colistin methansulfonate for treatment of carbapenem-resistant, colistin-susceptible A. baumannii infection which is very alarming data for the last backbone of treatment of MDR gram negative bacteria [8]". "Thus, the alarming spread of carbapenemases poses serious risk to these vulnerable patients, as only a few suboptimal therapeutic options remain available for treating such infections [9]". "Infections caused by carbapenem-resistant organisms have been associated with high mortality rates [5]"."Early detection and strict application of infection control measures have been reliable in reducing the likelihood of transmission in health care settings [10]". Therefore, the objective of this study was to characterize carbapenem resistance genes among GNB isolated from clinical samples from patients in one of the ICUs at Cairo University Hospital.

2. Materials and Methods

2.1. Study Design and Sample Collection

A prospective cross-sectional study was conducted over a period of 6 months (June to December 2013). Clinical samples were obtained from patients showing clinical evidence of infection at one surgical ICU of Cairo University Hospital. The research protocol was approved by the Research Ethics Committee of the Faculty of Medicine, Cairo University, Egypt.

2.2. Bacterial Isolates

A total of 211 samples were collected; 47 blood, 46 urine, 52 respiratory (sputum and bronchoalveolar lavage), 59 wound swabs, and seven fluid aspirates (pericardial, pleural, and ascitic). "Bacteria were isolated and identified by conventional microbiological methods [11]". "All suspected A. baumannii isolates were confirmed by PCR specifically designed to detect blaOXA-51-like genes, as described by Karmostaji et al. [12]".

2.3. Antimicrobial Susceptibility Testing

"The antimicrobial susceptibility profiles of the isolates were determined using a modified Kirby Bauer disc diffusion method on Muller Hinton agar (Oxoid Ltd., Basingstoke, UK) according to the guidelines of the Clinical and Laboratory Standards Institute (CLSI) [13]". The following antibiotic discs were used (Oxoid Ltd.): ampicillin (10 µg), one of the following β-lactam/β-lactamase inhibitors (amoxicillin/clavulanic acid, 30 µg; piperacillin/tazobactam, 110 µg), one of the first generation cephalosporins (cephalothin, 30 µg; cephalexin, 30 µg; cefazolin, 30 µg), one of the second generation cephalosporins (cefaclor, 30 µg; cefoxitin, 30 µg; cefixime, 5 µg), one of the third generation cephalosporins (cefoperazone, 75 µg; ceftazidime, 30 µg; cefotaxime, 30 µg; ceftriaxone, 30 µg), cefepime (30 µg), carbapenems (imipenem, 10 µg; meropenem, 10 µg), aminoglycosides (amikacin, 30 µg; gentamicin, 120 µg), one of the fluoroquinolones (ciprofloxacin, 5 µg; levofloxacin, 5 µg; ofloxacin, 5 µg), sulfamethoxazole-trimethoprim (25 µg), tigecycline (15 µg), polymyxin B (300 units), and colistin (10 µg).

2.4. Screening of Carbapenem-Resistant Isolates

"Isolates were screened for carbapenem resistance using an imipenem and meropenem disk diffusion method. Isolates were categorized as sensitive, intermediate, or resistant according to CLSI guidelines (CLSI, 2012) [13]". Isolates were tested for carbapenemase production by modified Hodge test (MHT) as described in the CLSI guidelines. MHT-positive K. pneumoniae ATCC1705 and MHT-negative K. pneumoniae ATCC1706 were used as control strains for the assay.

2.5. Genetic Characterization of Carbapenem-Resistant Isolates

All clinical isolates found to be resistant to imipenem or meropenem and/or positive by modified Hodge test were examined for the presence of blaKPC, blaOXA-48, and blaNDM-like genes by PCR. The PCR conditions and methodology were as described previously (14-16) (Table 1).

2.6. DNA Sequencing and Analysis

Any identified blaNDM genes were sequenced to determine the NDM variant of the enzyme using the primers listed in Table 1. PCR products were purified using a MinElute Gel Extraction Kit (Qiagen, Valencia, CA, USA). The purified PCR products were directly sequenced on both strands using a 310 Capillary Array Sequencer and Big Dye Terminator chemistry (Applied Biosystems, Foster City, CA, USA). NDM sequences were analyzed using the BioEdit Sequence Alignment Editor (Ibis Therapeutics, Carlsbad, CA, USA), and results were compared to a reference sequence (GenBank accession no. LC032101).

2.7. Statistical Analysis

All statistical analyses were performed using SPSS version 15 for Microsoft Windows (SPSS Inc., Chicago, IL, USA). Data were statistically described in terms of frequencies (number of cases) and percentages.

3. Results

A total of 229 GNB were isolated from the 211 samples, including 75 P. aeruginosa, 62 K. pneumoniae, 43 A. baumannii, 28 Escherichia coli, 13 Proteus mirabilis, three Proteus vulgaris, three Enterobacter spp., one Morganella morganii, and one Citrobacter spp. Of these, 50 isolates (21.8%) showed resistance to both imipenem and meropenem. Among the resistant isolates, only 29 isolates were positive by modified Hodge test. These carbapenem-resistant isolates included 23 A. baumannii, 13 K. pneumoniae, 13 P. aeruginosa, and 1 E. coli (Table 2). In total, 53.5% of the A. baumannii isolates showed resistance to carbapenems, versus 21% and 17.3% of K. pneumoniae and P. aeruginosa isolates, respectively.

When studying carbapenem-resistant isolates in relation to the site of infection, we found that respiratory infections yielded the highest number of carbapenem-resistant GNB (24, 48%), followed by wound infections (13, 26%) (Table 3). All 50 carbapenem-resistant isolates were MDR, with 100% resistance to ampicillin, β lactam/β-lactamase inhibitors, first, second, third, and fourth generation cephalosporins, and carbapenems. In addition, 49 (98%) isolates were resistant to trimethoprim-sulfamethoxazole, 41 (82%) were resistant to aminoglycosides, and 39 (78%) were resistant to fluoroquinolones. However, all isolates were sensitive to tigacycline, polymyxin B, and colistin. No specific patterns were detected in relation to the absence or presence of resistance genes.

PCR analysis revealed that none of the isolates carried blaKPC-like genes, while 24 of the 50 resistant isolates (48%) carried blaOXA-48-like genes, eight (16%) isolates carried blaNDM, and five (10%) carried both blaNDM and blaOXA-48-like genes (Table 4). Sequencing of the blaNDM genes revealed that all isolates contained the blaNDM-1 variant.

Table 1. Primers used for the detection of carbapenem resistance genes.

Gene Primer pair and sequence (5′–3′) Amplicon size
blaOXA-51-like OXA-51 Forward (5'-TAATGCTTTGATCGGCCTTG-3′), OXA-51 Reverse (5'-TGGATTGCACTTCATCTTG-3′)- 353 bp

Table 2. Number and percentage of carbapenem-resistant isolates among each species.

Isolated Gram-negative bacilli (no.) Number of isolates Number of carbapenem-resistant isolates Percentage of carbapenem-resistant isolates
Pseudomonas aeruginosa 75 13 17.3%
Klebsiella pneumoniae 62 13 21%
Acinetobacter baumannii 43 23 53.5%
Escherichia coli 28 1 3.57%
Proteus mirabilis 13 0 0%
Proteus vulgaris 3 0 0%
Enterobacter spp 3 0 0%
Morganella morganii 1 0 0%
Citrobacter spp 1 0 0%
Total 229 50 21.8%

Table 3. Distribution of carbapenem-resistant isolates according to site of infection.

  Blood No. (%) Urine No. (%) Respiratory samples No. (%) Wound swabs No. (%) Total No. (%)
Acinetobacter baumannii 3 (6%) 1 (2%) 13 (26%) 6 (12%) 23 (46%)
Klebsiella pneumoniae 2 (4%) 2 (4%) 5 (10%) 4 (8%) 13 (26%)
Pseudomonas aeruginosa 2 (4%) 3 (6%) 6 (12%) 2 (4%) 13 (26%)
Escherichia coli 0 (0%) 0 (0%) 0 (0%) 1 (2%) 1 (2%)
Total 7 (14%) 6 (12%) 24 (48%) 13 (26%) 50 (100%)

Table 4. Distribution of carbapenem resistance genes among tested isolates (no.=50).

  blaKPC No. (%) blaOXA-48 No. (%) blaNDM-1 No. (%) blaOXA-48 + blaNDM-1 No. (%)
Acinetobacter baumannii 0 (0%) 13 (26%) 3 (6%) 1 (2%)
Klebsiella pneumoniae 0 (0%) 8 (16%) 4 (8%) 4 (8%)
Pseudomonas aeruginosa 0 (0%) 2 (4%) 1 (2%) 0 (0%)
Escherichia coli 0 (0%) 1 (2%) 0 (0%) 0 (0%)
Total 0 (0%) 24 (48%) 8 (16%) 5 (10%)

4. Discussion

"In recent decades, the emergence of extended-spectrum β-lactamase-producing bacteria has led to increased use of carbapenems in clinical practice, which in turn has led to the emergence of isolates containing carbapenemases [4]". We screened GNB responsible for different clinical infections in patients admitted to one of the ICUs at Cairo University Hospital, and investigated carbapenemase production by these isolates. We identified 50 isolates with carbapenem resistance patterns among 229 isolated GNB (21.8%). Although P. aeruginosa and K. pneumoniae were the most commonly isolated species (75 and 62 respectively), A. baumannii isolates showed the highest incidence of carbapenem resistance (46%)." In agreement with these results, Fouad et al. identified 547 nosocomial infections in three ICUs from three different hospitals in Egypt between January 2011 and September 2012 and found that the majority of infections were caused by Klebsiella spp., whereas A. baumannii showed the highest levels of imipenem resistance (74%) [17]". "Our study also revealed that respiratory infections yielded the highest number of carbapenem-resistant organisms (48%). These results are in partial agreement with Maltezou et al., who investigated infections caused by carbapenem-resistant GNB in hospitalized children. They isolated 71 carbapenem-resistant pathogens causing infections in 65 children, of which 25 cases were diagnosed with pneumonia (35.2%) [18]".

Although KPC-producers are now being identified at an alarming rate across the USA, France, Israel, Greece, Colombia, and China, and outbreaks of KPC-producing bacteria have been reported in many European countries, South America, and India (19-21), we did not detect any blaKPC-like genes among the 50 isolates that were positive by phenotypic methods for carbapenemases production. "This is in agreement with findings reported by Shibl et al. [4]", who tested 60 K. pneumoniae isolates from Saudi Arabia (the majority of which were from patients in an ICU) and did not identify any blaKPC-like genes. Together, these results indicate that blaKPC-like genes are not the major source of carbapenemases in the Middle East.

"The carbapenem-hydrolyzing class D β-lactamase OXA-48 was first described in a K. pneumoniae strain isolated from Turkey in 2004, and is now endemic in Egypt (4). OXA-48 carbapenemases are also endemic in countries around the Mediterranean, and are rapidly spreading into other countries in Europe [22], [23]". "Although many reports have described patients becoming infected with strains carrying blaOXA-48-like genes during travel to Egypt [24], [25]", few surveillance studies have focused on this gene as a cause of carbapenem resistance in Egypt. "In a recent 6-month surveillance study of carbapenem-resistant GNB isolated from a cancer hospital in Egypt, only three isolates harbored this gene [26]". Our study identified a higher number of isolates (24 isolates) (Table 3) than previously reported, which may indicate the rapid spread of carbapenem resistance in Egypt through the dissemination of blaOXA-48-like genes. "Although blaOXA-48 is rarely detected in Acinetobacter spp., Goncalves et al. detected this gene in A. baumannii isolated from fecal flora of nursing home residents in northern Portugal [27]". "Importantly, blaOXA-48 is associated with transposons Tn1999 and Tn1999.2, which enable rapid transmission among GNB [28]".

"blaNDM-1 was initially identified in K. pneumoniae and E. coli recovered from a Swedish patient who was previously hospitalized in India, and has rapidly disseminated to other Enterobacteriaceae in several countries [29]". "NDM-producers are of particular concern as they also harbor multiple plasmid and chromosome-encoded resistance genes, resulting in a MDR phenotype [4]". "Recently, cases of NDM-producing A. baumannii have been described in Egypt, China, and Israel [20], [29], [30]". "Similar to blaOXA-48, the way in which blaNDM-1 has spread between GNB in Egypt is not yet clear, but some of the identified cases in Europe had a history of travelling to Egypt [30-32]". In this study, eight isolates were shown to harbor blaNDM-1 (Table 3), five of which also contained a blaOXA-48-like gene (four K. pneumoniae and one A. baumannii). "Although this pattern of combined resistance has been reported previously in Lebanon and Tunisia [3], [23]", the rates identified in the current study are alarmingly high: five isolates versus one K. pneumoniae isolate each in Lebanon and Tunisia. However, there is little published data discussing the effect of the coexistence of several carbapenemases in GNB, an issue that requires close and continuous monitoring in infected patients.

"The emergence of such resistant strains represents a significant threat, not only to our country, but globally, especially as the dissemination of resistance genes is hastened by high rates of immigration and tourism [4]". This study has documented the emergence of NDM-1- and OXA-48-positive GNB in Egypt. NDM and OXA-48 type carbapenemases are increasingly reported in our region, with the Middle East and North Africa now regarded as secondary reservoirs for these carbapenemases. Several alarming reports have described the introduction of OXA-48- and NDM-expressing GNB to some European countries by patients previously hospitalized in Egypt. Healthcare workers, especially in ICUs, need to be aware of the emergence of these MDR isolates, as they are a significant health concern. Enhanced surveillance and detection of these MDR pathogens is urgently required so that patients can be identified quickly and appropriate infection control measures can be instituted to stop further dissemination. Further studies are also needed to clarify the epidemiological features of carbapenemase-producing isolates in Egypt. Also what is very important is to activate the antimicrobial stewardship programs of which the most important is restriction of the big gun antibiotics like carbapenems, colistin, tigecyclin and vancomycin and restricting their prescription to privileged specialties like infectious disease, intensevists, and pulmologists which can authorize other specialties in patients their clinical situation necessitates these big gun antibiotics.

5. Conclusion

This study indicates that continuous surveillance of these multidrug-resistant pathogens is urgently required. And that is very important is to activate the antimicrobial stewardship programs of which the most important is restriction of the big gun antibiotics like carbapenems, colistin, tigecyclin and vancomycin and restricting their prescription to privileged specialties.

List of Abbreviations

Polymerase chain reaction (PCR);

Gram-negative bacilli (GNB);

Intensive care units (ICUs);

Multidrug-resistant (MDR);

Klebsiella pneumoniae carbapenemase (KPC);

Verona-Integron Mediated (VIM);

Instance plasmid-mediated (IMP);

New Delhi metallo-β-lactamases (NDM);

Expanded-spectrum oxacillinase (OXA);

Clinical and Laboratory Standards Institute (CLSI);

Modified Hodge test (MHT).


  1. Peleg AY, and Hooper DC. Hospital-Acquired Infections Due to Gram-Negative Bacteria. N Engl J 2010; 362 (19): 1804–1813.
  2. Magiorakos AP, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18: 268–281.
  3. Tamma PD, Cosgrove SE, Maragakis LL.Combination Therapy for Treatment of Infections with Gram-Negative Bacteria. Clin Microbiol Rev 2012; 25 (3): 450-470.
  4. Shibl A, Al-Agamy A, Memish, Z, Senok A, Abdul Khader S, Assiri A. The emergence of OXA-48- and NDM-1-positive Klebsiella pneumoniae in Riyadh, Saudi Arabia. International Journal of Infectious Diseases 2013; 17 (12): 1130–1133.
  5. Gupta N, Brandi M, Limbago BM, Jean B, Patel JB, Kallen, AJ. Carbapenem-Resistant Enterobacteriaceae: Epidemiology and Prevention. Clin Infect Dis 2011; 53 (1): 60-67.
  6. Rahal JJ. Antimicrobial Resistance among and Therapeutic Options against Gram-Negative Pathogens. Clin Infect Dis., Aug 15;49 Suppl 1:S4-S10. doi: 10.1086/599810.
  7. Mushi MF, Mshana SE, Imirzalioglu C, Bwanga F. Carbapenemase Genes among Multidrug Resistant Gram Negative Clinical Isolates from a Tertiary Hospital in Mwanza, Tanzania. BioMed Research International. vol. 2014, Article ID 303104, 6 pages, 2014. doi:10.1155/2014/303104.
  8. QureshiZA,HittleLE,O'HaraJA,RiveraJI,SyedA,ShieldsRK.Colistin-Resistant Acinetobacter baumannii: Beyond Carbapenem Resistance.Clin Infect Dis. (2015) 1; 60 (9): 1295-303.
  9. Ribeiro VB, Linhares AR, Zavascki AP, Barth AL. Performance of Quantification of Modified Hodge Test: An Evaluation with Klebsiella pneumoniae Carbapenemase-Producing Enterobacteriaceae Isolates,.BioMed Research International vol. 2014; Article ID 139305, 6 pages, 2014. doi:10.1155/2014/139305.
  10. Cohen MJ, Block C, Levin PD, et al. Institutional Control Measures to Curtail the Epidemic Spread of Carbapenem-Resistant Klebsiella pneumoniae: A 4-Year Perspective. Infect Control Hosp Epidemiol 2011; 32: 673-678.
  11. Schreckenberger PC, Janda JM, Wong JD. Algorism for identification of aerobic Gram negative bacilli. In: Murray, P.R., Baron, E.J., Jorgensen, J.H. et al. Manual of clinical microbiology 9th ed., Washington 2009; 26: 438-441.
  12. Karmostaji A, Peerayeh SN, Salmanian AH. Distribution of OXA-Type Class D β-Lactamase Genes among Nosocomial Multi Drug Resistant Acinetobacter baumannii Isolated in Tehran Hospitals. Jundishapur Journal of Microbiology 2013; 6 (5): e8219
  13. Clinical and Laboratory Standards Institute. 2012. Performance standards for antimicrobial susceptibility testing. 22nd informational supplement. Clinical and Laboratory Standards Institute document M100–S20. Wayne PA.
  14. Bratu S, Tolaney P, Karumudi U, et al.Carbapenemase-producing Klebsiella pneumonia in Brooklyn, N.Y.: molecular epidemiology and in vitro activity of polymyxin B and other agents.J. Antimicrob. Chemother 2005; 56:128-132.
  15. Aktaş Z, Kayacan CB, Schneider I, Can B, Midilli K, Bauernfeind A. Carbapenem hydrolyzing oxacillinase, OXA-48, persists in Klebsiella pneumonia in Istanbul, Turkey. Chemotheraphy 2008; 54: 101-106.
  16. Nordmann P, Naas T, Poirel L. Global spread of carbapenamase-producing Enterobacteriaceae. Emerg Infect Dis 2011; 17 (10): 1791-1798.
  17. Fouad M, Attia AS, Tawakkol WM, Hashem AM. Emergence of carbapenem-resistant Acinetobacter baumannii harboring the OXA-23 carbapenemase in intensive care units of Egyptian hospitals.Int J Infect Dis 2013; 17 (12): e1252-1254.
  18. Maltezou HC, Kontopidou F, Katerelos P, Daikos G, Roilides E, Theodoridou M. Infections caused by carbapenem-resistant Gram-negative pathogens in hospitalized children. Pediatr Infect Dis J 2013; 32 (4): e151-154.
  19. Arnold R, Thom KA, Sharma S, Phillips M, Johnson JK, Morgan DJ. Emergence of Klebsiella pneumoniae carbapenemase-producing bacteria. Southern Med J 2011; 104, (1): 40-45.
  20. Chen Y, Zhou Z, Jiang Y, Yu Y. Emergence of NDM-1-producing Acinetobacter baumannii in China. J. Antimicrob. Chemother 2011; 66: 1255–1259.
  21. Nordmann P, Poirel L, Carrër A, Toleman MA, Walsh TR.How To Detect NDM-1 Producers. J Clin Microbiol 2011a; 49 (2): 718–721.
  22. Levast M, Poirel L, Carrër A, et al.Transfer of OXA-48-positive carbapenem-resistant Klebsiella pneumoniae from Turkey to France. J Antimicrob Chemother 2011; 66: 944–945.
  23. Voulgari E, Zarkotou O, Ranellou K, Karageorgopoulos DE, Vrioni, G, Mamali V. Outbreak of OXA-48 carbapenemase- producing Klebsiella pneumoniae in Greece involving an ST11 clone. J Antimicrob Chemotherapy 2013; 68: 84–88.
  24. Espedido BA, Jason A, Ziochos H, et al. Whole Genome Sequence Analysis of the First Australian OXA-48-Producing Outbreak-Associated Klebsiella pneumonia Isolates: The Resistome and In Vivo Evolution. PLoS ONE 2013; 8 (3): e59920.
  25. Mataseje LF, Boyd DA, Hoang L, et al.Carbapenem-hydrolyzing oxacillinase-48 and oxacillinase-181 in Canada, 2011. Emerg Infect Dis 2013;. 19 (1): 157- 160.
  26. Poirel L, Abdelaziz MO, Bernabeu S, Nordmann P.Occurrence of OX A-48 and VIM-1 carbapenemase-producing Enterobacteriaceae in Egypt. International Journal of Antimicrobial Agents 2013; 41: 90–95.
  27. Goncalves D, Cecilio P, Ferreira H 2013. First detection of OXA-48-like-producing Acinetobacter baumannii in the faecal flora of nursing home residents in northernPortugal.abstr eP748 Abstr. 23rd Eur. Congr. Clin. Microbiol. Infect. Dis., Berlin, Germany
  28. Djahmi N, Dunyach-Remy C, Pantel A, Dekhil M, Sotto A, Lavigne JP. Epidemiology of Carbapenemase-Producing Enterobacteriaceae and Acinetobacter baumannii in Mediterranean Countries. BioMed Research International 2014. Hindawi Publishing Corporation BioMed Research International Volume 2014, Article ID 305784, 11 pages
  29. Espinal P, Fugazza G, López Y, et al.Dissemination of an NDM-2-Producing Acinetobacter baumannii Clone in an Israeli Rehabilitation Center. Antimicrob Agents Chemother 2011; 55 (11): 5396-5398.
  30. Kaase M, Nordmann P, Wichelhaus TA, Gatermann SG, Bonnin, RA, Poirel L. NDM-2 carbapenemase in Acinetobacter baumannii from Egypt. J. Antimicrob. Chemother 2011; 66: 1260–1262.
  31. Ghazawi A, Sonnevend A, Bonnin RA, Poirel A, Nordmann L, Hashmey P. NDM-2 carbapenemase-producing Acinetobacter baumannii in the United Arab Emirates. Clin Microbiol Infect 2012; 18: E34–E36.
  32. Hrabák J, Stolbová M, Studentová V, Fridrichová M, Chudáčková E, Zemlickova H. NDM-1 producing Acinetobacter baumannii isolated from a patient repatriated to the Czech Republic from Egypt, 2012 Feb 16. Euro Surveill; 17 (17),pii: 20085.

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