Overexpression of target enzyme gene fabI and efflux pump decrease triclosan susceptibility in Escherichia coli

Abstract Background: Escherichia coli isolates, the most opportunistic pathogen in the gut, are responsible for the most acquired infections. Triclosan is an effective disinfectant for inhibits microorganisms, but its widespread use causes its residue in urine, resulting in long-term exposure of E. coli in the intestine to triclosan environment and increasing triclosan resistance. We aim to provide the mechanism of action of E. coli isolates against triclosan and the molecular epidemiological analysis of triclosan-resistant strains.Results: Five triclosan-resistant isolates were screened out from 200 E. coli isolates by agar dilution method by to further study, interestingly, multidrug-resistant and cross-resistance phenotypes were observed in triclosan-resistant strains, but not in susceptible strains, and all except one exhibited an inhibition of efflux pump activity by efflux pump inhibition testing. Furthermore, compared with susceptible E. coli strain ATCC 25922, except fabI, increased expression were also found in efflux pump encoding genes ydcV, ydcU, ydcS, ydcT, cysP, yihV, acrB, acrD and mdfA in studied strains which had different PFGE patterns and STs types.Conclusions: These findings indicated that triclosan resistance in E. coli were mainly involved by overexpression of fabI gene, and there was a close association between overexpression of efflux pump with reducing susceptibility to triclosan. Besides, we described cross-resistance between triclosan and antibiotics may be related to the exposure time of triclosan.

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The prevalence and mechanism of triclosan resistance in Escherichia coli isolates from urine samples in Wenzhou, China

10.21203/rs.3.rs-24751/v1 ◽

2020 ◽

Author(s):

Weiliang Zeng ◽

Wenya Xu ◽

Ye Xu ◽

Wenli Liao ◽

Yajie Zhao ◽

...

Keyword(s):

Escherichia Coli ◽

Efflux Pump ◽

Cross Resistance ◽

Chain Reaction ◽

E Coli ◽

Resistant Strains ◽

Polymerase Chain ◽

Triclosan Resistance ◽

Encoding Genes

Abstract Background Widespread use of triclosan has been reported to cause its residue in urine, which provides an environment of long-term exposure to triclosan for intestinal Escherichia coli. We aimed to determine the triclosan and antibiotic resistance characteristics of Escherichia coli strains isolated from urine, and further investigate the resistance mechanism and molecular epidemic characteristics of triclosan resistant Escherichia coli isolates. Methods A total of 200 non-repetitive E. coli strains from urine samples were obtained and identified. The minimum inhibitory concentrations (MICs) of triclosan and antibiotics, fabI mutation, efflux pump activity, expression of 14 efflux pump encoding genes and epidemiological characteristics were detected with agar dilution method, polymerase chain reaction (PCR), carbonyl cyanide 3-chlorophenylhydrazone (CCCP) inhibition test, quantitative real-time polymerase chain reaction (RT-qPCR), multilocus sequence typing (MLST) and pulse field gel electrophoresis (PFGE) in all triclosan resistant isolates. Furthermore, we also investigated the effect of triclosan exposure in vitro on resistance in susceptible strains by serial passage experiment. Results Of 200 E. coli isolates, 2.5% (n = 5) were resistant to triclosan, multidrug resistance (MDR) and cross-resistance phenotypes were observed in these resistant strains, but not in susceptible strains. We did not observe any sense mutations within fabI gene in triclosan resistant strains. Moreover, except DC8603, all the others enhanced efflux pumps activity. Compared with ATCC 25922, except fabI, increased expression were also found in efflux pump encoding genes ydcV, ydcU, ydcS, ydcT, cysP, yihV, acrB, acrD and mdfA in studied strains with different PFGE patterns and STs types. Surprised, 5 susceptible E. coli isolates increased rapidly triclosan resistance only 4 days after exposure to subinhibitory triclosan concentration in vitro. Conclusions Our study is the first to be reported that short-term triclosan exposure in vitro increases triclosan resistance in susceptible E. coli isolates. Once strains have acquired resistance, they usually present MDR or cross-resistance phenotypes. Besides, our findings indicate that triclosan resistance were mainly involved by fabI overexpression in E. coli, and there was a close association between overexpression of efflux pumps with triclosan resistance.

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The prevalence and mechanism of triclosan resistance in Escherichia coli isolated from urine samples in Wenzhou, China

10.21203/rs.3.rs-24751/v2 ◽

2020 ◽

Author(s):

Weiliang Zeng ◽

Wenya Xu ◽

Ye Xu ◽

Wenli Liao ◽

Yajie Zhao ◽

...

Keyword(s):

Efflux Pump ◽

Urine Samples ◽

Cross Resistance ◽

Chain Reaction ◽

E Coli ◽

Resistant Strains ◽

Polymerase Chain ◽

Triclosan Resistance ◽

Encoding Genes

Abstract Background: The widespread application of triclosan contributes to its residual deposition in urine, which provides an environment of long-term exposure to triclosan for the intestinal Escherichia coli. We determined the triclosan and antibiotic resistance characteristics of E. coli strains isolated from urine samples and further investigated the resistance mechanism and molecular epidemic characteristics of triclosan-resistant E. coli isolates. Methods: A total of 200 non-repetitive E. coli strains were isolated from urine samples and then identified. The minimum inhibitory concentrations (MICs) of triclosan and antibiotics, fabI mutation, efflux pump activity, the expression of 14 efflux pump encoding genes, and epidemiological characteristics were determined by the agar dilution method, polymerase chain reaction (PCR), carbonyl cyanide 3-chlorophenylhydrazone (CCCP) inhibition test, quantitative real-time polymerase chain reaction (RT-qPCR), multilocus sequence typing (MLST), and pulse-field gel electrophoresis (PFGE) for all triclosan-resistant isolates. Furthermore, we also investigated the effect of triclosan exposure in vitro on antibiotic susceptibility and the efflux pump encoding gene expressions of triclosan-susceptible strains via serial passage experiments. Results: Of the 200 E. coli isolates, 2.5% (n = 5) were found to be resistant to triclosan, and multidrug resistance (MDR) and cross-resistance phenotypes were noted for these triclosan-resistant strains. The triclosan-sensitive strains also exhibited MDR phenotypes, probably because of the high resistance rate to AMP, CIP, LVX, and GEN. Gly79Ala and Ala69Thr amino acid changes were observed in the triclosan-resistant strains, but these changes may not mediate resistance of E. coli to triclosan, because mutations of these two amino acids has also been detected in triclosan-susceptible strains. Moreover, except for DC8603, all other strains enhanced the efflux pumps activity. As compared with ATCC 25922, except for fabI, increased expressions were noted for all efflux pump encoding genes such as ydcV, ydcU, ydcS, ydcT, cysP, yihV, acrB, acrD, and mdfA among the studied strains with varying PFGE patterns and STs types. Unexpectedly, 5 susceptible E. coli isolates showed rapidly increasing triclosan resistance after exposure to triclosan in vitro for only 12 days, while MDR or cross-resistance phenotypes and the overexpression of efflux pump genes were recorded among these triclosan-induced resistant isolates. Conclusions: This is the first study to report that short-term triclosan exposure in vitro increases triclosan resistance in susceptible E. coli isolates. After acquiring resistance, these strains may present MDR or cross-resistance phenotypes. Moreover, triclosan resistance mainly involves the overexpression of fabI and efflux pumps in E. coli isolates.

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The prevalence and mechanism of triclosan resistance in Escherichia coli isolated from urine samples in Wenzhou, China

Antimicrobial Resistance and Infection Control ◽

10.1186/s13756-020-00823-5 ◽

2020 ◽

Vol 9 (1) ◽

Author(s):

Weiliang Zeng ◽

Wenya Xu ◽

Ye Xu ◽

Wenli Liao ◽

Yajie Zhao ◽

...

Keyword(s):

Efflux Pump ◽

Urine Samples ◽

Cross Resistance ◽

Chain Reaction ◽

E Coli ◽

Resistant Strains ◽

Polymerase Chain ◽

Triclosan Resistance ◽

Encoding Genes

Abstract Background The widespread application of triclosan contributes to its residual deposition in urine, which provides an environment of long-term exposure to triclosan for the intestinal Escherichia coli. We determined the triclosan and antibiotic resistance characteristics of E. coli strains isolated from urine samples and further investigated the resistance mechanism and molecular epidemic characteristics of triclosan-resistant E. coli isolates. Methods A total of 200 non-repetitive E. coli strains were isolated from urine samples and then identified. The minimum inhibitory concentrations (MICs) of triclosan and antibiotics, fabI mutation, efflux pump activity, the expression of 14 efflux pump encoding genes, and epidemiological characteristics were determined by the agar dilution method, polymerase chain reaction (PCR), carbonyl cyanide 3-chlorophenylhydrazone (CCCP) inhibition test, quantitative real-time polymerase chain reaction (RT-qPCR), multilocus sequence typing (MLST), and pulse-field gel electrophoresis (PFGE) for all triclosan-resistant isolates. Furthermore, we also investigated the effect of triclosan exposure in vitro on antibiotic susceptibility and the efflux pump encoding gene expressions of triclosan-susceptible strains via serial passage experiments. Results Of the 200 E. coli isolates, 2.5% (n = 5) were found to be resistant to triclosan, and multidrug resistance (MDR) and cross-resistance phenotypes were noted for these triclosan-resistant strains. The triclosan-sensitive strains also exhibited MDR phenotypes, probably because of the high resistance rate to AMP, CIP, LVX, and GEN. Gly79Ala and Ala69Thr amino acid changes were observed in the triclosan-resistant strains, but these changes may not mediate resistance of E. coli to triclosan, because mutations of these two amino acids has also been detected in triclosan-susceptible strains. Moreover, except for DC8603, all other strains enhanced the efflux pumps activity. As compared with ATCC 25922, except for fabI, increased expressions were noted for all efflux pump encoding genes such as ydcV, ydcU, ydcS, ydcT, cysP, yihV, acrB, acrD, and mdfA among the studied strains with varying PFGE patterns and STs types. Unexpectedly, 5 susceptible E. coli isolates showed rapidly increasing triclosan resistance after exposure to triclosan in vitro for only 12 days, while MDR or cross-resistance phenotypes and the overexpression of efflux pump genes were recorded among these triclosan-induced resistant isolates. Conclusions This is the first study to report that short-term triclosan exposure in vitro increases triclosan resistance in susceptible E. coli isolates. After acquiring resistance, these strains may present MDR or cross-resistance phenotypes. Moreover, triclosan resistance mainly involves the overexpression of fabI and efflux pumps in E. coli isolates.

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Triclosan resistance in clinical isolates of Acinetobacter baumannii

Journal of Medical Microbiology ◽

10.1099/jmm.0.008524-0 ◽

2009 ◽

Vol 58 (8) ◽

pp. 1086-1091 ◽

Cited By ~ 38

Author(s):

Yagang Chen ◽

Borui Pi ◽

Hua Zhou ◽

Yunsong Yu ◽

Lanjuan Li

Keyword(s):

Acinetobacter Baumannii ◽

Efflux Pump ◽

Resistance Mechanism ◽

Dilution Method ◽

Agar Dilution Method ◽

Active Efflux ◽

Low Level ◽

High Level ◽

Resistance Rates ◽

Triclosan Resistance

The susceptibility to triclosan of 732 clinical Acinetobacter baumannii isolates obtained from 25 hospitals in 16 cities in China from December 2004 to December 2005 was screened by using an agar dilution method. Triclosan MICs ranged between 0.015 and 16 mg l−1, and the MIC90 was 0.5 mg l−1, lower than the actual in-use concentration of triclosan. Twenty triclosan-resistant isolates (MICs ≥1 mg l−1) were characterized by antibiotic susceptibility, clonal relatedness, fabI mutation, fabI expression, and efflux pump phenotype and expression to elucidate the resistance mechanism of A. baumannii to triclosan. The resistance rates of triclosan-resistant isolates to imipenem, levofloxacin, amikacin and tetracycline were higher than those of triclosan-sensitive isolates. Triclosan resistance was artificially classified as low level (MICs 1–2 mg l−1) or high level (MICs ≥4 mg l−1). High-level triclosan resistance could be explained by a Gly95Ser mutation of FabI, whilst wild-type fabI was observed to be overexpressed in low-level resistant isolates. Active efflux did not appear to be a major reason for acquired triclosan resistance, but acquisition of resistance appeared to be dependent on a background of intrinsic triclosan efflux.

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BaeR participates in cephalosporins susceptibility by regulating the expression level of outer membrane proteins in Escherichia coli

The Journal of Biochemistry ◽

10.1093/jb/mvaa100 ◽

2020 ◽

Author(s):

Shuaiyang Wang ◽

Chunbo You ◽

Fareed Qumar Memon ◽

Geyin Zhang ◽

Yawei Sun ◽

...

Keyword(s):

Escherichia Coli ◽

Membrane Proteins ◽

Outer Membrane ◽

Efflux Pump ◽

Outer Membrane Proteins ◽

Expression Level ◽

Antibiotics Resistance ◽

Dilution Method ◽

Expression Levels ◽

E Coli

Abstract The two-component system BaeSR participates in antibiotics resistance of Escherichia coli. To know whether the outer membrane proteins involve in the antibiotics resistance mediated by BaeSR, deletion of acrB was constructed and the recombined plasmid p-baeR was introduced into E. coli K12 and K12△acrB. Minimum inhibitory concentrations (MICs) of antibacterial agents were determined by 2-fold broth micro-dilution method. Gene expressions related with major outer membrane proteins and multidrug efflux pump-related genes were determined by real-time quantitative reverse transcription polymerase chain reaction. The results revealed that the MICs of K12ΔacrB to the tested drugs except for gentamycin and amikacin decreased 2- to 16.75-folds compared with those of K12. When BaeR was overexpressed, the MICs of K12ΔacrB/p-baeR to ceftiofur and cefotaxime increased 2.5- and 2-fold, respectively, compared with their corresponding that of K12△acrB. At the same time, the expression levels of ompC, ompF, ompW, ompA and ompX showed significant reduction in K12ΔacrB/p-baeR as compared with K12△acrB. Moreover, the expression levels of ompR, marA, rob and tolC also significantly ‘decreased’ in K12ΔacrB/p-baeR. These findings indicated that BaeR overproduction can decrease cephalosporins susceptibility in acrB-free E. coli by decreasing the expression level of outer membrane proteins.

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Plasmid mediated colistin resistant mcr-1 and co-existence of OXA-48 among Escherichia coli from clinical and poultry isolates: first report from Nepal

Gut Pathogens ◽

10.1186/s13099-020-00382-5 ◽

2020 ◽

Vol 12 (1) ◽

Cited By ~ 1

Author(s):

Bijaya Muktan ◽

Upendra Thapa Shrestha ◽

Binod Dhungel ◽

Bagish Chandra Mishra ◽

Nabaraj Shrestha ◽

...

Keyword(s):

Escherichia Coli ◽

Resistance Gene ◽

Diffusion Method ◽

Dilution Method ◽

Agar Dilution Method ◽

Colistin Resistance ◽

Clinical Specimens ◽

E Coli ◽

Resistant Genes ◽

Rectal Swabs

Abstract Background Plasmid-mediated resistance to the last-resort drugs: carbapenems and colistin is an emerging public health threat. The studies on the prevalence and co-expression of resistant genes among livestock and human pathogens are rare in Nepal. This is the first study in Nepal exploring the prevalence and co-existence of colistin resistance gene, mcr-1 along with carbapenemase resistance gene, OXA-48 in Escherichia coli isolated from poultry and clinical specimens. Methods A total of 240 rectal swabs from chickens of five different poultry farms of Kathmandu valley and 705 mid-stream urine samples from human subjects attending Kantipur Hospital, Kathmandu were collected between August, 2018 and March, 2019. Rectal swabs and urine specimens were cultured. E. coli isolated from the specimens were screened for antimicrobial susceptibility testing (AST) using disk diffusion method’. Minimum inhibitory concentration (MIC) of colistin was determined by agar dilution method using 0.5 µg/ml to 32 µg/ml. The E. coli isolates were first screened for mcr-1 followed by screening for OXA-48 genes using conventional Polymerase chain reaction (PCR). Results Of the total samples analyzed, E. coli was isolated from 31.7% (76/240) of poultry and 7.9% (56/705) of clinical specimens. In AST, 80% (61/76) of E. coli from poultry and 79% (44/56) from clinical specimens were MDR. The phenotypic prevalence of colistin resistance in poultry specimens were 31.6% (24/76) and clinical specimens were 21.4% (12/56). In PCR assay, 27.6% (21/76) of poultry and 19.6% (11/56) of clinical isolates had colistin resistant mcr-1 gene. MICs value of E. coli isolates ranged from 4 to 32 (µg/ml) in both clinical and poultry isolates. Prevalence of co-existing carbapenem resistance gene, OXA-48, among colistin resistant mcr-1 positive isolates was 38% (8/21) in poultry specimens and 18.2% (2/11) in clinical specimens. Conclusions The high prevalence of colistin and carbapenem resistant genes, and their co-existence in plasmid DNA of E. coli isolates in this study suggests the possible spread to other animal, human and environmental pathogens. Molecular methods in addition to the conventional diagnostics in laboratories can help in early diagnosis, effective management and control of their potential transmission.

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Mutation in 23S rRNA Associated with Macrolide Resistance in Neisseria gonorrhoeae

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.46.9.3020-3025.2002 ◽

2002 ◽

Vol 46 (9) ◽

pp. 3020-3025 ◽

Cited By ~ 104

Author(s):

Lai-King Ng ◽

Irene Martin ◽

Gary Liu ◽

Louis Bryden

Keyword(s):

Neisseria Gonorrhoeae ◽

Promoter Region ◽

Efflux Pump ◽

Macrolide Resistance ◽

23S Rrna ◽

Cross Resistance ◽

E Coli ◽

Single Base Pair ◽

Resistant Strains ◽

Domain V

ABSTRACT Fifty-six azithromycin-resistant (MICs, 2.0 to 4.0 μg/ml) Neisseria gonorrhoeae strains with cross-resistance to erythromycin (MICs, 2.0 to 64.0 μg/ml), isolated in Canada between 1997 and 1999, were characterized, and their mechanisms of azithromycin resistance were determined. Most (58.9%) of them belonged to auxotype-serotype class NR/IB-03, with a 2.6-mDa plasmid. Based on resistance to crystal violet (MICs ≥ 1 μg/ml), 96.4% of these macrolide-resistant strains appeared to have increased efflux. Nine of the eleven strains selected for further characterization were found to have a promoter region mtrR mutation, a single-base-pair (A) deletion in the 13-bp inverted repeat, which is believed to cause overexpression of the mtrCDE-encoded efflux pump. The two remaining macrolide-resistant strains (erythromycin MIC, 64.0 μg/ml; azithromycin MIC, 4.0 μg/ml), which did not have the mutation in the mtrR promoter region, were found to have a C2611T mutation (Escherichia coli numbering) in the peptidyltransferase loop in domain V of the 23S rRNA alleles. Although mutations in domain V of 23S rRNA alleles had been reported in other bacteria, including E. coli, Streptococcus pneumoniae, and Helicobacter pylori, this is the first observation of these mutations associated with macrolide resistance in N. gonorrhoeae.

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Detection of Plasmid-Mediated Colistin Resistant mcr-1 Gene in Escherichia coli Isolated from Infected Chicken Livers in Nepal

Animals ◽

10.3390/ani10112060 ◽

2020 ◽

Vol 10 (11) ◽

pp. 2060

Author(s):

Sayara Bista ◽

Upendra Thapa Shrestha ◽

Binod Dhungel ◽

Pragya Koirala ◽

Tulsi Ram Gompo ◽

...

Keyword(s):

Escherichia Coli ◽

Conventional Polymerase Chain Reaction ◽

Diffusion Method ◽

Dilution Method ◽

Agar Dilution Method ◽

Human Pathogens ◽

Colistin Resistance ◽

Disk Diffusion Method ◽

E Coli ◽

Agar Dilution

Background: Plasmid-mediated resistance to the colistin in poultry is considered as an emerging problem worldwide. While poultry constitutes the major industry in Nepal, there is a paucity of evidence on colistin resistance in Escherichia coli isolates causing natural infections in poultry. This study aimed to explore the prevalence of plasmid-mediated colistin resistance gene, mcr-1 in E. coli isolated from liver samples of dead poultry suspected of E. coli infections. Methods: A total of two hundred and seventy liver samples (227 broilers and 43 layers) from dead poultry suspected of colibacillosis were collected from post-mortem in the Central Veterinary Laboratory (CVL), Kathmandu, between 1 February and 31 July 2019. The specimens were processed to isolate and identify E. coli; an antimicrobial susceptibility test (AST) using disk diffusion method was performed with 12 different antibiotics: Amikacin (30 µg), ampicillin (10 µg), ciprofloxacin (5 µg), chloramphenicol (30 µg), cefoxitin (30 µg), ceftazidime (30 µg), ceftriaxone (30 µg), cotrimoxazole (25 µg), gentamicin (10 µg), imipenem (10 µg), levofloxacin (5 µg) and tetracycline (30 µg). Colistin resistance was determined by agar dilution method and colistin-resistant strains were further screened for plasmid-mediated mcr-1 gene, using conventional polymerase chain reaction (PCR). Results: Out of 270 liver samples, 53.3% (144/270) showed growth of E. coli. The highest number (54%; 109/202) of E. coli isolates was obtained in the liver samples from poultry birds (of both types) aged less than forty days. In AST, 95.1% (137/144) and 82.6% (119/144) of E. coli isolates were resistant against tetracycline and ciprofloxacin, respectively, while 13.2% (19/144) and 25.7% (37/144) isolates were resistant to cefoxitin and imipenem, respectively. In the same assay, 76.4% (110/144) E. coli isolates were multi-drug resistant (MDR). The phenotypic prevalence of colistin resistance was 28.5% (41/144). In the PCR assay, 43.9% (18/41) of colistin-resistant isolates were screened positive for plasmid-mediated mcr-1. Conclusion: The high prevalence of mcr-1 in colistin-resistant E. coli isolates in our study is a cause of concern for the probable coming emergence of colistin resistance in human pathogens, due to horizontal transfer of resistant genes from poultry to human isolates.

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No Decrease in Susceptibility to NVC-422 in Multiple-Passage Studies with Methicillin-Resistant Staphylococcus aureus, S. aureus, Pseudomonas aeruginosa, and Escherichia coli

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.05985-11 ◽

2012 ◽

Vol 56 (5) ◽

pp. 2753-2755 ◽

Cited By ~ 13

Author(s):

Louisa D'Lima ◽

Lisa Friedman ◽

Lu Wang ◽

Ping Xu ◽

Mark Anderson ◽

...

Keyword(s):

Escherichia Coli ◽

Staphylococcus Aureus ◽

Pseudomonas Aeruginosa ◽

Fusidic Acid ◽

Methicillin Resistant Staphylococcus Aureus ◽

Cross Resistance ◽

Methicillin Resistant ◽

Content Type ◽

E Coli ◽

Resistant Strains

ABSTRACTTwenty-five serial passages ofEscherichia coli,Pseudomonas aeruginosa, andStaphylococcus aureusand 50 passages of methicillin-resistantStaphylococcus aureusresulted in no significant increase in NVC-422 MICs, while ciprofloxacin MICs increased 256-fold forE. coliand 32-fold forP. aeruginosaandS. aureus. Mupirocin, fusidic acid, and retapamulin MICs for MRSA increased 64-, 256-, and 16-fold, respectively. No cross-resistance to NVC-422 was observed with mupirocin-, fusidic acid-, and retapamulin-resistant strains.

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ANTIMICROBIAL ACTIVITY OF METHANOL EXTRACT FROM STEM BARK OF Cinnamomum sintoc

Jurnal Natural ◽

10.24815/jn.v0i0.8049 ◽

2017 ◽

Vol 17 (2) ◽

pp. 77

Author(s):

Nurdin Saidi ◽

Hira Helwati ◽

Lailatul Qhadariah Lubis ◽

Muhammad Bahi

Keyword(s):

Escherichia Coli ◽

Antimicrobial Activity ◽

Antibacterial Activity ◽

Methanol Extract ◽

Stem Bark ◽

Dilution Method ◽

Agar Dilution Method ◽

E Coli ◽

Paper Disk ◽

Agar Dilution

Antimicrobial activity of methanol extract from stem bark of Cinnamomum sintoc has been evaluated against Candida albicans, Staphylococcus aureus and Escherichia coli. The extraction of compound was carried out by maceration, then isolation by column chromatograph, which yielded five (5) subfractions (A-E). Activity against fungus C. albicans, S. aureus bacteria dan E. coli using agar dilution method in paper disk. Methanol extract was not potent against antifungal activity but shows antibacterial activity with medium category. Subfraction C showed that antibacterial activity against S. aureus and E. coli with weak category, but subfractions D and E did not show any activity.

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