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ORIGINAL ARTICLE  
Year : 2017  |  Volume : 60  |  Issue : 2  |  Page : 196-201
Phenotypic and molecular characterization of cefotaximases, temoniera, and sulfhydryl variable β-lactamases in Pseudomonas and Acinetobacter isolates in an Indian tertiary health-care center


1 Department of Microbiology, J. N. Medical College and Hospital, A. M. U., Aligarh; Department of Microbiology, Integral Institute of Medical Sciences and Research, Lucknow, Uttar Pradesh, India
2 Department of Microbiology, J. N. Medical College and Hospital, A. M. U., Aligarh, Uttar Pradesh, India; Department of Microbiology, Immunology and Infectious Diseases, College of Medicine and Medical Sciences, Arabian Gulf University, Kingdom of Bahrain
3 Department of Microbiology, J. N. Medical College and Hospital, A. M. U., Aligarh, Uttar Pradesh, India; Faculty of Public Health and Tropical Medicine, Jazan University, Kingdom of Saudi Arabia
4 Department of Microbiology, J. N. Medical College and Hospital, A. M. U., Aligarh, Uttar Pradesh, India

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Date of Web Publication19-Jun-2017
 

   Abstract 

Background: Cefotaximases (CTX-M), temoniera (TEM), and sulfhydryl variable (SHV) constitute a rapidly growing cluster of enzymes that have disseminated geographically. They are spreading to species other than Enterobacteriaceae and might be responsible for the presence of blaCTX-M,blaTEM, and blaSHVgenes in Pseudomonas and Acinetobacter spp. The present study was designed to characterize CTX-M, TEM, and SHV phenotypically and genotypically in Pseudomonas and Acinetobacter spp. Materials and Methods: A total of 90 isolates (73 Pseudomonas and 17 Acinetobacter spp.), resistant to any of the third-generation cephalosporins, were randomly selected from clinical samples. Results: Of 90 isolates, 64 (71.11%) were tested positive for extended-spectrum β-lactamase (ESBL) production. Among phenotypically tested ESBL producers, forty isolates were randomly selected for molecular characterization. The prevalence of CTX-M, TEM, and SHV was found to be 57.5%, 15%, and 75%, respectively. Multiplex polymerase chain reaction assay categorized blaCTX-Mgenes into Groups 1 and 26 where Group 1 was present in only 5 isolates and Group 25 was present in rest of the 18 isolates. Conclusion: This is among the premier systemic reports from India documenting phenotypic and molecular characterization of CTX-M, TEM, and SHV β-lactamases in Pseudomonas and Acinetobacter spp. With judicious use of antibiotics and strict infection control procedures, it may be possible to limit the effects of these newer β-lactamases.

Keywords: Acinetobacter, cefotaximases, polymerase chain reaction, Pseudomonas, sulfhydryl variable, temoniera

How to cite this article:
Jamali S, Shahid M, Sobia F, Singh A, Khan HM. Phenotypic and molecular characterization of cefotaximases, temoniera, and sulfhydryl variable β-lactamases in Pseudomonas and Acinetobacter isolates in an Indian tertiary health-care center. Indian J Pathol Microbiol 2017;60:196-201

How to cite this URL:
Jamali S, Shahid M, Sobia F, Singh A, Khan HM. Phenotypic and molecular characterization of cefotaximases, temoniera, and sulfhydryl variable β-lactamases in Pseudomonas and Acinetobacter isolates in an Indian tertiary health-care center. Indian J Pathol Microbiol [serial online] 2017 [cited 2022 Jan 24];60:196-201. Available from: https://www.ijpmonline.org/text.asp?2017/60/2/196/208377



   Introduction Top


Third-generation (extended-spectrum) cephalosporins are often used to treat infections caused by Gram-negative bacteria. Only a few years after their introduction in the early 1980s, however, enzymes that hydrolyze third-generation cephalosporins (ceftazidime, cefotaxime, and ceftriaxone) and other β-lactam antibiotics except the cephamycins and carbapenems were described. Since then, extended-spectrum β-lactamase (ESBL)-producing bacteria have been recognized as important causes of nosocomial infections.[1],[2]

The first plasmid-mediated β-lactamase in Gram-negatives, temoniera-1 (TEM-1), was reported in 1965 from an Escherichia coli isolate belonging to a patient in Athens, Greece, named temoniera (hence the designation TEM).[3] The TEM-1 β-lactamase has spread worldwide and is now found in different species of members of Enterobacteriaceae, Pseudomonas aeruginosa, Haemophilus influenzae, and Neisseria gonorrhoeae.[4] A Klebsiella ozaenae isolate from Germany possessed a β-lactamase, sulfhydryl variable-2 (SHV-2), which efficiently hydrolyzed cefotaxime and to a lesser extent ceftazidime.[5] Some β-lactamases have hydrolytic profiles similar to those of the TEM and SHV mutants but their evolutionary history is different, and these non-TEM and non-SHV plasmid-mediated class A ESBLs have been reported as cefotaximases (CTX-M). These enzymes hydrolyze cephalothin better than benzylpenicillin and they preferentially hydrolyze cefotaxime over ceftazidime.

The early SHV and TEM variants have been largely replaced by the CTX-M family of ESBLs. However, the first two CTX-M enzymes were identified at approximately the same time in the early 1990s in Western Europe and South America in individual clinical isolates.[6],[7] Within a decade, the CTX-M β-lactamases became the predominant ESBL family in many medical centers such that they have largely replaced most of the TEM- and SHV-derived ESBLs throughout the world.[8],[9],[10] Five different clusters of CTX-Ms (CTX-M-1, CTX-M-2, CTX-M-8, CTX-M-9, and CTX-M-25) have been recognized on the basis of their amino acid sequences (http://www.lahey.org/studies/webt.stm).

It is believed that recombination events have also helped in evolution and diversification of CTX-M-β-lactamase. CTX-M enzymes are spreading to species other than Enterobacteriaceae and might be responsible for the presence of blaCTX-M genes in P. aeruginosa and Acinetobacter spp., which has been observed in recent surveillance studies.[11] The first description of the presence of CTX-M ESBLs in P. aeruginosa and Stenotrophomonas maltophilia was reported by Al Naiemi et al. in the year 2006.[12]

The present study was designed to characterize CTX-M, TEM, and SHV β-lactamases phenotypically as well as genotypically in Pseudomonas and Acinetobacter spp., as their documentation in these organisms is lacking in India.


   Materials and Methods Top


Various clinical specimens including pus, urine, blood, CSF, ear swab, conjunctival swab, and semen that were received for routine culture and susceptibility testing in the clinical microbiology laboratory, J. N. Medical College, Aligarh, during a period of 1 year (October 2010 to September 2011), were studied. A total of 90 isolates, of these, 73 Pseudomonas spp. and 17 Acinetobacter spp., that were resistant to any of the third-generation cephalosporins, were randomly selected from clinical samples to study for the presence of β-lactamases.

Phenotypic extended-spectrum β-lactamase detection by double-disk synergy test

Phenotypic ESBL detection was carried out by double-disk synergy test (DDST) using ceftazidime (30 μg), cefotaxime (30 μg), and piperacillin/tazobactam (100/10 μg) disks.[13] In this method, inoculums containing test organism of 0.5 McFarland turbidity were streaked onto a Mueller-Hinton agar plate with the help of swab sticks. Piperacillin/tazobactam disk was placed in the center of the plate whereas disks containing cefotaxime (30 μg) and ceftazidime (30 μg) were placed 20 mm from center to center from piperacillin-tazobactam disk and plates were incubated overnight at 37°C. The test organism is considered to produce ESBL if the zone size around the test antibiotic disk increases toward the piperacillin-tazobactam disk [Figure 1].
Figure 1: Double-disk synergy test: Organism showing enhanced zone of inhibition between ceftazidime and cefotaxime and piperacillin/tazobactam containing disk indicating extended-spectrum β-lactamase production

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Molecular characterization

Among ESBL producers, 40 isolates (37 Pseudomonas and 3 Acinetobacter spp.) were randomly selected for molecular characterization.

DNA template preparation

For proper extraction of genes, bacterial DNA template was prepared from freshly cultured bacterial strains by scraping 2–3 colonies from the agar plate and suspending them in 50 μl of molecular grade water. The suspension was then exposed to heating at 95°C for 5 min, followed by immediately chilling at 4°C.

Polymerase chain reaction

Multiplex polymerase chain reaction (PCR) was carried out to characterize isolates, for the presence of specific groups of CTX-M, as described previously by Woodford et al.[14] with some modifications. These forty isolates were also subjected to monoplex PCR to detect the presence of blaTEM and blaSHV genes by PCR protocol as described previously.[15] Genes were amplified by the primer set, which span universal region. Primers were synthesized by Operon Biotechnologies, Cologne, Germany. [Table 1],[Table 2],[Table 3] show the reagents required for the preparation of reaction mixture to detect blaCTX-M,blaTEM, and blaSHV genes, respectively.
Table 1: Detection of cefotaximases groups by multiplex polymerase chain reaction

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Table 2: Detection of blaTEM

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Table 3: Detection of blaSHV

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Previously characterized isolates provided by Prof. Daniel Jonas, Germany, were used as positive controls.

Cycling conditions

For detection of blaCTX-M

The PCR was carried out in a thermal cycler (MJ-mini Bio-Rad, USA) with an initial denaturation at 94°C for 5 min, followed by forty cycles of final denaturation at 94°C for 1 min. Annealing at 52°C for 60 s, initial extension at 72°C for 1 min, and final extension at 72°C for 10 min.

For detection of blaTEM and blaSHV

Initial denaturation at 94°C for 3 min, followed by thirty cycles of final denaturation at 94°C for 30 s. Annealing at 64°C for 30 s, extension at 72°C for 1 min, and final elongation at 72°C for 10 min.

DNA fragments were visualized by Bio-Rad Gel documentation system (Bio-Rad, USA).


   Results Top


All the ninety isolates of Pseudomonas and Acinetobacter spp. suspected to be potential ESBL producer were tested by DDST using piperacillin/tazobactam, for ESBL detection, where tazobactam acted as an inhibitor. Of 90 isolates, 64 (71.11%) were tested positive for ESBL production while remaining isolates did not show synergy.

Among phenotypically tested ESBL producers, forty isolates were randomly selected for molecular characterization. Isolates were subjected to PCR to confirm the presence of blaCTX-M gene. Multiplex PCR was carried out to detect plasmid-mediated CTX-M β-lactamases. In multiplex PCR, 23 (57.5%) out of forty isolates were found to be positive for blaCTX-M genes. 22 (59.46%) isolates of Pseudomonas spp. and 1 (33.33%) isolate of Acinetobacter spp. were found to harbor blaCTX-M genes. Multiplex PCR assay categorized blaCTX-M genes into Groups 1 and 25, where Group 1 was present in only five isolates and Group 25 was present in rest of the 18 isolates [Figure 2].
Figure 2: Electrophoretogram (on 2% agarose) showing results of multiplex polymerase chain reaction for the detection of blaCTX-Malleles. Lanes 1 and 15 are showing ladders (Genei high range DNA ruler). Lane 2 shows positive control strain for Group 1. Lanes 3 and 5–12 show test strains positive for Group 25 whereas Lane 4 shows negative isolate. Lanes 13 and 14 are showing amplicons belonging to Group 1 family

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Apart from CTX-M, the study isolates of Pseudomonas and Acinetobacter spp. were also tested for the presence of TEM and SHV β-lactamases at the genetic level by PCR [Figure 3] and [Figure 4]. Although 6 (16.22%) strains of Pseudomonas spp. were found to be positive for TEM, none of the isolates of Acinetobacter spp. were found to have TEM β-lactamase. Taking into consideration both types of strains, the overall prevalence of TEM β-lactamase reduced to 15%. On the other hand, 29 (78.38%) isolates of Pseudomonas spp. and 1 (33.33%) isolate of Acinetobacter spp. were found to carry SHV-type ESBL. Hence, of total 40 isolates, 30 (75%) were found to carry blaSHV genes.
Figure 3: 2% agarose gel is showing amplification pattern of temoniera-type gene. Lanes M are showing Fermentas high range DNA ruler. Lane 1 shows positive control strain for temoniera. Lanes 2–5 show clinical isolates harboring temoniera genes while Lanes 6 and 7 show negative isolates

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Figure 4: 2% agarose gel is showing amplification pattern of sulfhydryl variable type gene. Lane M is showing high range DNA ruler (Genei, Bengaluru). Lane 1 shows positive control strain for sulfhydryl variable whereas Lane 2 shows negative control. Lanes 3–7 show clinical isolates harboring sulfhydryl variable genes

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   Discussion Top


Although a few studies have reported the prevalence of ESBL producers in Indian hospitals, ESBL-producing bacteria may have evolved in several hospitals all over the country. ESBL detection is not commonly carried out in many microbiology units in developing countries, India included. This could be attributed to lack of awareness and lack of resources and facilities to conduct ESBL identification. In recent years, there has been an increased incidence and prevalence of ESBLs. For a number of reasons, the detection of ESBL producing strains is of significant importance for all major hospitals worldwide. First, these strains are most likely to be even more prevalent than it is currently recognized. Hence, we have conducted phenotypic as well as molecular characterization of selected clinical isolates.

The prevalence of ESBL producers varies across continents and countries and also within hospitals. In our study isolates, we observed 71.11% ESBL producers by phenotypic detection method, which is much higher than other studies. DDST, being negative in suspected ESBL-producing strains, could be due to coexistence of other β-lactamases such as AmpC β-lactamase, because inhibitor which is used in the DDST test for the ESBL detection may act as an inducer of the high-level AmpC production. Hence, even if ESBL is present, it will not be detected and it may result in a false negative test. The previous studies from India have reported ESBL production (based on phenotypic detection only) varying from 12.6% to 81%.[16],[17] Taneja et al. have reported the ESBL production in 36.5% isolates, and among these, the maximum occurrence was noted in Klebsiella spp. (51.2%), followed by E. coli(40.2%), Enterobacter aerogenes (33.4%), and P. aeruginosa (27.9%).[18] 20.27% of P. aeruginosa isolates were found to be positive for ESBL production in a study conducted by Aggarwal et al.[19] The prevalence of ESBL-producing Acinetobacter spp. was found to be 75% by Anita et al.[20] In India (Sikkim), Tsering et al. reported the prevalence of ESBL to be 34.03%.[21] E. coli(26.15%), Klebsiella pneumoniae (57.14%), P. aeruginosa (32.61%), P. mirabilis (42.86%), M. morganii (71.43%), and C. freundii (50%) were found to be ESBL-positive by DDST. Umadevi et al. have reported ESBL production in 81% E. coli, 74% K. pneumonia, and 14% Pseudomonas isolates from Puducherry.[17] In a study reported by Goel et al., in 2013, ESBL was produced by 42.30% of P. aeruginosa and 17.95% of A. baumannii isolates.[22] Recently, among nonfermenters (Pseudomonas and Acinetobacter), Kamalraj et al. from Tamil Nadu reported 38.3% to be ESBL producers.[23] Similar study from Tanzania performed by Stephen Mshana et al. reported specific ESBL rates among K. pneumoniae, Escherichia coli, Acinetobacter spp., Proteus spp., and other enterobacteria as 63.7%, 24.4%, 17.7%, 6.4%, and 27.9%, respectively.[24]

In the present study, among class A ESBLs, the highest frequency was noted for blaSHV (75%), followed by blaCTX-M (57.5%). The least occurrence was observed for TEM, which was just 15%. Multiplex PCR assay categorized most of the blaCTX-M genes into Group 25. This finding is in contrast to various other reports over enterobacterial isolates, where Group 1 shares the maximum percentage. This could be due to the difference in the type of organisms selected for study as we have included Pseudomonas and Acinetobacter spp. for analysis, which are nonfermenters. Molecular detection was negative in some of the chosen strains. This could be due to the fact that these isolates may be harboring different ESBL types than ESBL tested in this study.

As reported by Baby Padmini et al., 19 out of 23 isolates of K. pneumoniae yielded positive amplicons for blaCTX-M genes and only 1 out of 3 isolates was positive for SHV-specific primers.[25] Kaur and Aggarwal from northern India demonstrated CTX-M, SHV, and TEM Genes in 44%, 10.7%, and 3.2% of enterobacterial isolates.[26] Nandagopal et al. reported CTX-M in 96.8% of the uropathogenic strains, followed by TEM in 24.2% and SHV in 4.8% of the strains by PCR.[27] Recently, Saxena et al. reported blaCTX genes in seven out of 24 isolates of P. aeruginosa by PCR.[28]blaCTX-M-2 was detected in five isolates and blaCTX-M-1 was detected in two isolates. Hussain et al., from Pakistan, have reported the maximum prevalence of blaCTX-M (57.7%), followed by blaTEM (20.3%) and blaSHV (15.4%) in E. coli isolates.[29] These studies are contrast to our report as we have found SHV in the majority of the isolates, followed by CTX-M and TEM.

The presence of blaCTX-M-2, in P. aeruginosa, is believed to be a result of their transfer from Enterobacteriaceae.[30] The high prevalence of K. pneumoniae harboring blaCTX-M-2 in the same hospital was reported in 2011 by Tollentino et al., and this may have been the reservoir for horizontal transmission.[31] Polotto et al., from Brazil, reported blaCTX-M-2 to be the most prevalent ESBL gene (19.6%) in P. aeruginosa.[32] Recently, in a study conducted at Iran, among P. aeruginosa isolates, 30 (100%), 2 (6.6%), and 0 (0%) amplified the blaTEM,blaSHV, and blaCTX-M genes, respectively.[33]


   Conclusion Top


Early detection of β-lactamases is need of time to counteract their dissemination. Our study is among the premier systemic reports from India documenting phenotypic as well as molecular characterization of CTX-M, TEM, and SHV β-lactamases in Pseudomonas and Acinetobacter spp. With judicious use of antibiotics and strict infection control procedures, it may be possible to limit the effects of these newer β-lactamases. This study would help to provide vital information to health care givers needed to address problem of emerging antibiotic resistance.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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Correspondence Address:
Sana Jamali
Department of Microbiology, Integral Institute of Medical Sciences and Research, Lucknow, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.208377

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    Figures

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    Tables

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