Medical and Dental Consultantsí Association of Nigeria
Home - About us - Editorial board - Search - Ahead of print - Current issue - Archives - Submit article - Instructions - Subscribe - Advertise - Contacts - Login 
  Users Online: 1437   Home Print this page Email this page Small font sizeDefault font sizeIncrease font size
 

  Table of Contents 
ORIGINAL ARTICLE
Year : 2018  |  Volume : 21  |  Issue : 2  |  Page : 176-182

Resistance Pattern and Detection of Metallo-beta-lactamase Genes in Clinical Isolates of Pseudomonas aeruginosa in a Central Nigeria Tertiary Hospital


Department of Medical Microbiology, National Hospital Abuja, Abuja, Nigeria

Date of Acceptance26-Oct-2017
Date of Web Publication21-Feb-2018

Correspondence Address:
Dr. K O Zubair
Department of Medical Microbiology, National Hospital Abuja, Abuja
Nigeria
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_229_17

Rights and Permissions
   Abstract 


Background: Acquired metallo-β-lactamases (MBLs) pose serious problem both in terms of treatment and infection control in the hospitals and report across the world showed an increase in their prevalence. However, there is a paucity of data from Africa, and their report is rare in Nigeria. Aim: This study aimed to determine the prevalence of acquired MBL-resistant genes in carbapenem-resistant Pseudomonas aeruginosa in Abuja, North Central Nigeria. Materials and Methods: Two hundred nonduplicate, consecutive isolates of P. aeruginosa from clinical samples submitted to the Medical Microbiology Laboratory of National Hospital, Abuja were screened for carbapenem resistance using imipenem and meropenem. Phenotypic detection of MBL-producing strains was determined using Total MBL confirm kits and E-test strips on isolates that were resistant to both Imipenem and meropenem. The MBL genes were detected using multiplex polymerase chain reaction, while the gene variant was determined by sequencing. Results: Twenty-two MBL-producing strains were detected phenotypically, but only 5 harbored the blaVIM-1 gene, giving a prevalence of 2.5%. These 5 strains were resistant to all the antipseudomonal antibiotics tested except Aztreonam and Colistin. Other common MBL-genes were not detected. Conclusion: The prevalence of MBL-producing strains of P. aeruginosa which poses serious challenge for therapeutics and infection control is currently low in Abuja, North Central, Nigeria. Therefore, rational use of the carbapenems and other antipseudomonal antibiotics, regular surveillance and adequate infection control measures should be instituted to limit further spread.

Keywords: Abuja, carbapenem-resistance, metallo-β-lactamases, Pseudomonas aeruginosa


How to cite this article:
Zubair K O, Iregbu K C. Resistance Pattern and Detection of Metallo-beta-lactamase Genes in Clinical Isolates of Pseudomonas aeruginosa in a Central Nigeria Tertiary Hospital. Niger J Clin Pract 2018;21:176-82

How to cite this URL:
Zubair K O, Iregbu K C. Resistance Pattern and Detection of Metallo-beta-lactamase Genes in Clinical Isolates of Pseudomonas aeruginosa in a Central Nigeria Tertiary Hospital. Niger J Clin Pract [serial online] 2018 [cited 2022 Aug 14];21:176-82. Available from: https://www.njcponline.com/text.asp?2018/21/2/176/225937




   Introduction Top


Pseudomonas aeruginosa, an organism widespread in nature, is an important cause of healthcare-associated infection, especially in patients with compromised host defense.[1],[2],[3],[4] Its infections are associated with relatively high treatment failures and mortality due to its intrinsic and acquired resistance to commonly available antibiotics, particularly in patients hospitalized with burns, malignancies, and those with cystic fibrosis, as well as in those with fulminant infections such as sepsis and pneumonia, most of which are fatal with high mortality rate, often >50%.[5],[6]

With increasing inappropriate use of antimicrobials both in human and veterinary medicine, microorganisms are rapidly evolving from susceptible into resistant strains to various antibiotics with consequent therapeutic failures [7],[8],[9] At present, a number of pathogenic bacteria are being described as multidrug-resistant (MDR), extensively-drug-resistant, or pan-drug-resistant pathogens because they have developed or acquired resistance to a number of clinically useful antibiotics.[7],[10],[11]P. aeruginosa has been identified in all the three categories.

The carbapenems used to be the empirical agent of last resort when dealing with MDR Gram-negative bacteria, but there are increasing reports of resistance to them, especially in P. aeruginosa. In Nigeria, different researchers in Zaria, Lagos, and Kano have reported P. aeruginosa carbapenem resistance of between 20% and 60% using phenotypic methods of Detection.[12],[13],[14] This organism employs different mechanisms such as reduced outer membrane permeability, target site modification, efflux pumps over-expression, expression of chromosomal AmpC β-lactamases, and the acquisition of β-lactamases to become resistant to this group of antibiotics.[15],[16] Of all these, the most worrisome is the emergence of strains of P. aeruginosa with acquired metallo-β-lactamases (MBLs) which present the most clinically challenging situation both in terms of treatment and infection control.[17]

MBLs are carbapenemases with capability of hydrolyzing the penicillins, cephalosporins, cephamycins, and the carbapenems but not monobactams.[18] In addition, pathogens that harbor MBL genes tend to carry co-resistance genes for other classes of antibiotics. MBL genes are usually borne on mobile genetic elements such as integrons, transposons, plasmids, or associated with insertion sequences which confer it with the propensity to spread not just within a species but also between different species. MBLs have been reported in more than 28 species of Gram-negative bacteria from more than forty countries.[19] The mortality attributable to infections caused by MBL-producing P. aeruginosa is estimated to range from 70% to 90%.[5],[6]

Since resistance is driven by antibiotics use,[20],[21] there is increasing report of these strains, and the possibility of rising prevalence exist with escalating use of the carbapenems as they become more available for clinical use, even as better methods of detection of MBL producing strain are becoming available in clinical microbiology laboratories. A number of studies in Nigeria have reported antibiotics resistance in P. aeruginosa, but, there is a paucity of data on MBL-induced resistance.[1],[3],[12],[19],[22],[23],[24],[25] In Abuja, the federal capital territory of Nigeria, neither the prevalence rate of MBL-producing strains of P. aeruginosa nor the MBL gene type harbored by any of such strains has been reported.

This study was carried out to determine the prevalence of MBL-producing strains of P. aeruginosa in a tertiary health-care setting in Abuja as well as characterize the common resistance gene-types harbored by the strains as a way of generating local data for planning and advocacy with respect to empiric therapy, antibiotic stewardship, and infection control.


   Materials and Methods Top


This was a cross-sectional study carried out over a 34-month period ranging from February 2013 to November 2015 at the National Hospital Abuja (NHA), a 400-bed tertiary health-care institution located in Abuja, North Central Region of Nigeria. Two hundred consecutive, nonduplicate, isolates of P. aeruginosa from all samples except stool submitted to the Medical Microbiology Laboratory of NHA were identified using standard techniques,[26] and further subjected to a temperature of 42 °C to eliminate the other members of the fluorescence group of Pseudomonads. Antibiotics Susceptibility Testing was performed using Modified Kirby–Bauer disc diffusion method, in accordance with the CLSI standards. Antibiotics tested were piperacillin/tazobactam, ceftazidime, cefepime, aztreonam, imipenem, meropenem, gentamicin, amikacin, ciprofloxacin, and colistin. P. aeruginosa that showed resistance to imipenem and or meropenem were subjected to phenotypic MBL confirmation using Total MBL Confirm Kit from ROSCO Diagnostica (ROSCO Diagnostica A/S, Taastrupgaardsvej, Denmark) in accordance with the manufacturer's instructions. The sensitivity and specificity of total MBL confirm kit from ROSCO Diagnositica is 97.7% and 100%, respectively.[27] Further confirmation of MBLs was done with E-test strip from Liofilchem (Liofilchem, Roseto degli Abruzzi, Italy). A positive MBL test is indicated by the ratio of the MIC of IMP: IMD or MRP: MRD ≥8 (IMP/IMD ≥8 or MRP/MRD ≥8) or the presence of a phantom zone. P. aeruginosa ATCC 27853 was used as control strain for these procedures. Phenotypically confirmed MBL producers were stored at 20°C in 50% glycerol stock until they were further analyzed at the DNA Labs, Kaduna, for molecular confirmation. Using the following primers: blaIMP- types, blaVIM- types, blaGIM-1, blaSPM-1, blaSIM-1 and blaNDM-1, multiplex polymerase chain reaction (PCR) was used to detect the specific type of MBL gene harbored by the MBL-producing strains of P. aeruginosa. In addition, one pair of class 1 integron primer was included to detect the presence of class 1 integron. DNA sequencing using Bechmann coulter CEQ-8000 (Beckman Coulter, Kraemer Boulevard, Brea, CA, USA) was carried out on sample No. 22. The resulting nucleotide sequence was analyzed using the BLAST program on NCBI website (http://blast.ncbi.nlm.nih.gov/Blast.cgi) which shows the nucleotide sequence as 99% identical to blaVIM-1 gene with E-value of 6 × 10−180 and accession numbers KF975369 in the GenBank. This resulting nucleotide sequence was used as the positive control for the multiplex PCR while all the PCR reaction mixture without a primer was used as negative control as shown in [Figure 1] in the result section.
Figure 1: Agarose gel electrophoresis result for multiplex polymerase chain reaction product for the detection of metallo-β-lactamase genes. Lane 1 = Strain no: 10, 5 = 54, 13 = 112, 20 = 152, 22 = 185. PC: Positive Control, NC: Negative Control. NB: The bands in lane 1, 5, 13, 20, and 22 are the specific (positive) bands while the second band in lane 5 is a nonspecific band which should be ignored

Click here to view


Ethical approval was given by the Ethical Committee of NHA while informed consent was obtained from patient using standard consent form.


   Results Top


Distribution of clinical samples/isolates

The 200 isolates of P. aeruginosa from various clinical samples were distributed as follows: wound swab/biopsy 103 (51.5%); ear swab 32 (16%); urine 27 (13.5%); and blood culture 20 (10%) [Table 1].
Table 1: Distribution of isolates of P. aeruginosa in various clinical samples

Click here to view


Antibiotics susceptibility profile of Pseudomonas aeruginosa

Of the 200 isolates 176 (88%), 169 (84.5%), 168 (84%), and 146 (73%) were susceptible to imipenem, piperacillin/tazobactam, colistin, and cefepime, respectively [Table 2]. In addition, 139 (69.5%) isolates were susceptible to amikacin, 133 (66.5%) to gentamicin, 135 (67.5%) to ciprofloxacin, and 128 out of the 178 tested (71.9%) susceptible to meropenem. One hundred and two isolates (51%) were resistant to ceftazidime.
Table 2: Susceptibility of P. aeruginosa isolates to antipseudomonal antibiotics

Click here to view


Multiplex polymerase chain reaction result of metallo-β-lactamases-Pseudomonas aeruginosa and resistant pattern

Out of the 22 phenotypically detected MBL-P. aeruginosa, the blaVIM-1 gene was detected in only five [5] [Table 3]. The agarose gel electrophoresis result for the blaVIM-1 gene is shown in [Figure 1].
Table 3: Microbiological and molecular characteristics of Carbapenem-Resistance P. aeruginosa isolates

Click here to view



   Discussion Top


Antibiotics susceptibility profile

Results of antibiotics susceptibility testing revealed that isolates of P. aeruginosa were most susceptible to imipenem, piperacillin-tazobactam, colistin, and cefepime but were largely resistant to ceftazidime. The previous retrospective studies conducted in this center also showed that imipenem had the highest susceptibility against P. aeruginosa in the range of 80%–90%, but with reduced susceptibility to ceftazidime, one-third-generation cephalosporin that was heavily relied on for its antipseudomonal activity.[28],[29],[30],[31] The concordance of the retrospective studies with this prospective one implies that there has been little or no change in the antibiotics susceptibility pattern of P. aeruginosa between 2010 and 2015 in this locality.

The studies, however, revealed that ceftazidime could no longer be suitable as an agent for empiric therapy in serious infections suspected to be caused by P. aeruginosa. Ceftazidime has been the “workhorse” for the treatment of severe infections caused by P. aeruginosa in many tertiary healthcare institutions in Nigeria for over two decades, and this may account for the high resistance profile. This reduced susceptibility to ceftazidime and other commonly prescribed antipseudomonal antibiotics had previously been reported in studies from other tertiary health-care institutions in other parts of Nigeria.[23],[24],[26],[32] Similar reason stated above may be adduced for these susceptibility patterns. However, a well-designed multicenter research may provide more representative data.

Imipenem and the carbapenems generally, are not commonly prescribed in our center, implying less exposure and pressure on this pathogen to these antibiotics; hence, the relatively high susceptibility profile. Similarly, piperacillin-tazobactam, cefepime, and colistin are not commonly prescribed, were not usually included in routine antibiotics susceptibility testing as reflected in the retrospective studies. Therefore, on the basis of this susceptibility profile, imipenem and piperacillin/tazobactam, would appear to be the most appropriate choices for empiric therapy in the treatment of patients with serious infections in which P. aeruginosa is suspected while colistin and cefepime should be reserved as last drugs of choice. Notwithstanding, the commonly prescribed antipseudomonal agents are still clinically useful, provided their selection is based on an appropriate antibiogram and regular surveillance.

Prevalence of VIM-1 metallo-β-lactamases-Pseudomonas aeruginosa

Although the phenotypic method used in this study detected 22 (11%) MBL-producing P. aeruginosa strains, only five were found to harbor the gene for MBLs when subjected to molecular analyses, and they were all blaVIM-1 sub-types. This gave an overall prevalence of 2.5%. This, to the best of our knowledge, is the first report of the detection of blaVIM-1 in clinical isolate of carbapenem resistance P. aeruginosa in Nigeria. The multiplex PCR did not detect the MBL gene for IMP, NDM, SPM, SIM, and GIM that were assayed for. Most published studies on the detection of MBLs in P. aeruginosa in Nigeria were limited to phenotypic methods only.[14],[33],[34],[35] Studies in Kaduna/Kano, Lagos, and Calabar using the ethylenediaminetetraacetic acid (EDTA) disc synergy method gave prevalence of 21.2%,[14] 8.8%[34] and 4.1%,[36] respectively; whereas an Enugu study gave a prevalence of 10%,[33] similar to the 11% in this study. The differences in the methods used partly accounted for the wide differences in prevalence as the EDTA disc synergy method is of lower specificity than the disc potentiating method used in this and the Enugu studies.

The phenotypic resistance to carbapenems in the absence of relevant genes for their enzyme elaboration, most probably suggests that resistant mechanisms other than MBLs could be at play in the isolates. Efflux pumps, impermeability of the outer membranes, modification of target site and carbapenemases other than MBLs may also mediate carbapenem resistance in P. aeruginosa.[15],[16]

Interestingly, the findings in this study are a marked contrast from a similar study in Kenya [37] where all phenotypically detected MBL-producing, carbapenem-resistant P. aeruginosa (CRPA) harbored the blaVIM-2 gene, which is the much more common one while our study detected the much rarer blaVIM-1 gene, suggesting that this is the dominant strain circulating in Abuja, Nigeria. It would appear that blaVIM-2 does not presently exist in Abuja and probably Nigeria as a whole; an issue for further studies for conclusive determination.

The blaVIM-1 was first reported in Verona University Hospital, Italy, in 1999 by Laura Lauretti et al. in an isolate of CRPA.[38] Subsequently, it was frequently reported around the Mediterranean region and has largely remained confined there.[39],[40] Its detection in Abuja may be a case of imported antibiotic resistance strains because many Nigerians frequently visit this region for pilgrimage (Israel, Saudi Arabia, Rome), medical tourism, and work. Two cases of imported MBL-producing P. aeruginosa from Ghana to Norway [41] and from Egypt to Hungary [42] have previously been reported and serve to illustrate this phenomenon. These two cases represented the first report of MBL-producing P. aeruginosa harboring blaVIM-2 gene in Norway and Hungary, a scenario which highlighted the significant role of international travel on the spread of antimicrobial resistance across the globe.

blaNDM-1 which has been linked with international travel, especially to the Indian Subcontinent, where it is commonly found, surprisingly was not detected in this study despite the fact that many Nigerians, particularly the inhabitants of Abuja, travel to India for medical care. Although blaNDM-1 gene had been more commonly reported among Enterobacteriaceae than Pseudomonas, the result of this study runs contrary to the common assertion that blaNDM-1 has great propensity for international dissemination as a consequence of international travel, especially to India. It is also possible that the rare blaVIM-1 detected in this study developed de novo.

The strains of P. aeruginosa isolated in this study that harbored blaVIM-1 gene was resistant to all the antipseudomonal antibiotics tested except aztreonam and colistin, but two (strains No. 10 and 185) were also resistant to aztreonam which may be due to additional resistant mechanisms. This reduced susceptibility to a broad array of antipseudomonal antibiotics has been reported by the previous studies and has a grave clinical implication for health care.[38],[40]

Although it has been reported that blaVIM genes are usually carried on gene cassettes inserted on a Class 1 integron,[40],[43] it was not found in this study because the Class 1 integron primers used during the multiplex PCR reaction did not detect it.


   Conclusion Top


Acquired MBL-producing strains of P. aeruginosa poses serious challenge for therapy as well infection control. However, the prevalence rate is currently low in Abuja, North Central Nigeria as reported in this study. With some harbouring the rare blaVIM-1-gene. Hence, rational use of antipseudomonal antibiotics, good infection control practice should be instituted to curb further spread of these strains.

Limitation of study

The limitation of this study was a result of limited resources and time constraint. Other genes responsible for MBL resistance and other mechanisms of resistance in these strains of P. aeruginosa could have been detected using whole gene sequencing. Similarly, gene localization, gene cassette array, and genetic relatedness are information that could be derived from these strains where resources are available.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Oni AA, Ewete AF, Gbaja AT, Kolade AF, Mutiu WB, Adeyemo DA, et al. Mini review nosocomial infections: Surgical site infection in UCH Ibadan, Nigeria. Niger J Surg Res 2006;8:19-23.  Back to cited text no. 1
    
2.
Samuel SO, Kayode OO, Musa OI, Nwigwe GC, Aboderin AO, Salami TA, et al. Nosocomial infections and the challenges of control in developing countries. Afr J Clin Exp Microbiol 2010;11:102-10.  Back to cited text no. 2
    
3.
Atata RF, Ibrahim YK, Akanbi AA 2nd, Olurinola PF, Sani A. Prevalence of nosocomial infections in a tertiary health care institution in Nigeria (2000-2002): A retrospective study. J Appl Environ Sci 2006;2:212-5.  Back to cited text no. 3
    
4.
Chollom SC, Agada GO, Gotep JG, Mwankon SE, Okwori AJ. Short communication: Bacteriological profile of infected surgical sites in Jos, Nigeria. Malays J Microbiol 2012;8:285-8.  Back to cited text no. 4
    
5.
Cornaglia G, Giamarellou H, Rossolini GM. Metallo-β-lactamases: A last frontier for β-lactams? Lancet Infect Dis 2011;11:381-93.  Back to cited text no. 5
[PUBMED]    
6.
Zavascki AP, Barth AL, Gonçalves ALS, Moro LD, Fernandes JF, Martin AF, et al. The influence of metallo-β-lactamase production on mortality in nosocomial Pseudomonas aeruginosa infections. J Antimicrob Chemother 2006;58(2):387-392  Back to cited text no. 6
    
7.
Paphitou NI. Antimicrobial resistance: Action to combat the rising microbial challenges. Int J Antimicrob Agents 2013;42 Suppl:S25-8.  Back to cited text no. 7
    
8.
Uchil RR, Kohli GS, Katekhaye VM, Swami OC. Strategies to combat antimicrobial resistance. J Clin Diagn Res 2014;8:ME01-4.  Back to cited text no. 8
    
9.
Leung E, Weil DE, Raviglione M, Nakatani H, World Health Organization World Health Day Antimicrobial Resistance Technical Working Group. The WHO policy package to combat antimicrobial resistance. Bull World Health Organ 2011;89:390-2.  Back to cited text no. 9
    
10.
Giske CG, Monnet DL, Cars O, Carmeli Y, ReAct-Action on Antibiotic Resistance. Clinical and economic impact of common multidrug-resistant gram-negative bacilli. Antimicrob Agents Chemother 2008;52:813-21.  Back to cited text no. 10
    
11.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, 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;18:268-81.  Back to cited text no. 11
    
12.
Olayinka AT, Onile BA, Olayinka BO. Prevalence of multi-drug resistant (MDR) Pseudomonas aeruginosa isolates in surgical units of Ahmadu Bello university teaching hospital, Zaria, Nigeria: An indication for effective control measures. Ann Afr Med 2004;3:13-6.  Back to cited text no. 12
    
13.
Smith S, Ganiyu O, John R, Fowora M, Akinsinde K, Odeigah P, et al. Antimicrobial resistance and molecular typing of Pseudomonas aeruginosa isolated from surgical wounds in Lagos, Nigeria. Acta Med Iran 2012;50:433-8.  Back to cited text no. 13
    
14.
Yusuf I, Yusha'u M, Sharif AA, Getso MI, Yahaya H, Bala JA, et al. Detection of metallo-β- lactamases among gram negative bacterial isolates from Murtala Muhammed specialist hospital Kano and Almadina hospital Kaduna, Nigeria. Bayero J Pure Appl Sci 2012;5:84-8.  Back to cited text no. 14
    
15.
Livermore DM. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: Our worst nightmare? Clin Infect Dis 2002;34:634-40.  Back to cited text no. 15
    
16.
Hancock RE, Speert DP. Antibiotic resistance in pseudomonas aeruginosa: Mechanisms and impact on treatment. Drug Resist Updat 2000;3:247-55.  Back to cited text no. 16
    
17.
Meletis G, Bagkeri M. Pseudomonas aeruginosa: Multi-drug-resistance development and treatment options. Infect Control 2013;:33-56.  Back to cited text no. 17
    
18.
Zhao WH, Hu ZQ. Epidemiology and Genetics of VIM-type Metallo-β-Lactamases in Gram-Negative Bacilli; 2011. Available from: http://www.medscape.com/viewarticle/740371_1. [Last updated on 2011 Mar 01; Last accessed on 2014 Oct 15].  Back to cited text no. 18
    
19.
Jombo GT, Jonah P, Ayeni JA. Multiple resistant Pseudomonas aeruginosa in contemporary medical practice: Findings from urinary isolates at a Nigerian University Teaching Hospital. Niger J Physiol Sci 2008;23:105-9.  Back to cited text no. 19
    
20.
Austin DJ, Kristinsson KG, Anderson RM. The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci U S A 1999;96:1152-6.  Back to cited text no. 20
    
21.
Weinstein RA. Controlling antimicrobial resistance in hospitals: Infection control and use of antibiotics. Emerg Infect Dis 2001;7:188-92.  Back to cited text no. 21
    
22.
Ogbolu DO, Ogunledun A, Adebiyi OE, Daini OA, Alli AO. Antibiotic susceptibility patterns of Pseudomonas aeruginosa to available antipseudomonal drugs in Ibadan, Nigeria. Afr J Med Med Sci 2008;37:339-44.  Back to cited text no. 22
    
23.
Olayinka AT, Olayinka BO, Onile BA. Antibiotic susceptibility and plasmid pattern of Pseudomonas aeruginosa from the surgical unit of a university teaching hospital in North central Nigeria. Int J Med Med Sci 2009;1:79-83.  Back to cited text no. 23
    
24.
Ozumba UC. Antibiotic sensitivity of isolates of Pseudomonas aeruginosa in Enugu, Nigeria. Afr J Clin Exp Microbiol 2003;4:48-51.  Back to cited text no. 24
    
25.
Kehinde AO, Ademola SA, Okesola AO, Oluwatosin OM, Bakare RA. Pattern of bacterial pathogen in burn wound infections in Ibadan, Nigeria. Ann Burns Fire Disasters 2004;17:12-5.  Back to cited text no. 25
    
26.
Washington W, Stephen A, William J, Elmer K, Gary P, Paul SG. Processing specimen. In: Koneman's Color Atlas and Textbook of Diagnostic Microbiology. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2006. p. 27-39.  Back to cited text no. 26
    
27.
Yong D, Lee Y, Jeong SH, Lee K, Chong Y. Evaluation of double-disk potentiation and disk potentiation tests using dipicolinic acid for detection of metallo-β-lactamase-producing Pseudomonas spp. and Acinetobacter spp. J Clin Microbiol 2012;50:3227-32.  Back to cited text no. 27
    
28.
Iregbu KC, Eze S. Pseudomonas aeruginosa infections in a tertiary hospital in Nigeria. Afr J Clin Exp Microbiol 2015;16:33-6.  Back to cited text no. 28
    
29.
Iregbu KC, Nwajiobi-Princewil PI. Urinary tract infections in a tertiary hospital in Abuja, Nigeria. Afr J Clin Exp Microbiol 2013;14:169-73.  Back to cited text no. 29
    
30.
Iregbu KC, Uwaezuoke NS, Nwajiobi-Princewill IP, Eze So, Medugu N, Shettima S, et al. A profile of wound infections in National Hospital Abuja. Afr J Clin Exp Microbiol 2013;14:160-3.  Back to cited text no. 30
    
31.
Iregbu KC, Sonibare S. Profile of infections in Intensive Care Unit (ICU) in a central Nigeria tertiary hospital. Afr J Clin Exp Microbiol 2015;16:23-7.  Back to cited text no. 31
    
32.
Fadeyi A, Akanbi AA 2nd, Nwabuisi C, Onile BA. Antibiotic disc sensitivity pattern of Pseudomonas aeruginosa isolates obtained from clinical specimens in Ilorin, Nigeria. Afr J Med Med Sci 2005;34:303-6.  Back to cited text no. 32
    
33.
Chika E, Malachy U, Ifeanyichukwu I, Peter E, Thaddeus G, Charles E. Phenotypic detection of metallo – β – lactamase (MBL) enzyme in Enugu, Southeast Nigeria. Am J Biol Chem Pharm Sci 2014;2:1-6.  Back to cited text no. 33
    
34.
Eyo AA, Asuquo AE, Epoke J. Detection of Pseudomonas aeruginosa isolates producing Metallo-beta-lactamases in Southern Nigeria Hospitals. In: ICAAC. University of Calabar: ASM; 2013. p. C2-1596. Available from: http://www.icaaconline.com. [Last accessed on 2015 Jun 12].  Back to cited text no. 34
    
35.
Ikpeme EM, Nfongeh JF, Akubuenyi FC, Etim LB, Eyi-Idoh KH. Prevalence of metallo-β-lactamase-producing Pseudomonas aeruginosa isolated from hospitalized elderly individuals with urinary tract infections. Transnatl J Sci Technol 2012;2:50-6.  Back to cited text no. 35
    
36.
Aibinu I, Nwanneka T, Odugbemi T. Occurrence of ESBL and MBL in clinical isolates of Pseudomonas aeruginosa from Lagos, Nigeria. J Am Sci 2007;3:81-5.  Back to cited text no. 36
    
37.
Pitout JD, Revathi G, Chow BL, Kabera B, Kariuki S, Nordmann P,et al. Metallo-beta-lactamase-producing Pseudomonas aeruginosa isolated from a large tertiary centre in Kenya. Clin Microbiol Infect 2008;14:755-9.  Back to cited text no. 37
    
38.
Lauretti L, Riccio ML, Mazzariol A, Cornaglia G, Amicosante G, Fontana R, et al. Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother 1999;43:1584-90.  Back to cited text no. 38
    
39.
Bush K, Jacoby G. PTimothy. ß-Lactamase classification and amino acid sequences for tem, shv and oxa extended-spectrum and inhibitor resistant enzymes. Lahey Clin 2015. Available from: http://www.lahey.org/studies/other.asp/[table 1]. [Last updataed on 2015 Oct 22; Last accessed on 2015 Nov 24].  Back to cited text no. 39
    
40.
Hong DJ, Bae IK, Jang IH, Jeong SH, Kang HK, Lee K, et al. Epidemiology and characteristics of metallo-β-lactamase-producing Pseudomonas aeruginosa. Infect Chemother 2015;47:81-97.  Back to cited text no. 40
    
41.
Samuelsen O, Buarø L, Toleman MA, Giske CG, Hermansen NO, Walsh TR, et al. The first metallo-beta-lactamase identified in Norway is associated with a TniC-like transposon in a Pseudomonas aeruginosa isolate of sequence type 233 imported from ghana. Antimicrob Agents Chemother 2009;53:331-2.  Back to cited text no. 41
    
42.
Szabó D, Szentandrássy J, Juhász Z, Katona K, Nagy K, Rókusz L, et al. Imported PER-1 producing Pseudomonas aeruginosa, PER-1 producing Acinetobacter baumanii and VIM-2-producing Pseudomonas aeruginosa strains in hungary. Ann Clin Microbiol Antimicrob 2008;7:12.  Back to cited text no. 42
    
43.
Queenan AM, Bush K. Carbapenemases: The versatile beta-lactamases. Clin Microbiol Rev 2007;20:440-58.  Back to cited text no. 43
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
  
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed3226    
    Printed72    
    Emailed0    
    PDF Downloaded441    
    Comments [Add]    

Recommend this journal