scholarly journals Multidrug-Resistant Avian Pathogenic Escherichia coli Strains and Association of Their Virulence Genes in Bangladesh

2020 ◽  
Vol 8 (8) ◽  
pp. 1135
Author(s):  
Otun Saha ◽  
M. Nazmul Hoque ◽  
Ovinu Kibria Islam ◽  
Md. Mizanur Rahaman ◽  
Munawar Sultana ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Virulence Genes ◽  
Multidrug Resistant ◽  
Avian Pathogenic Escherichia Coli ◽  
E Coli ◽  
Molecular Approaches ◽  
Clade B ◽  
Pathogenic Escherichia Coli ◽  
Resistance Patterns

The avian pathogenic Escherichia coli (APEC) strains are the chief etiology of colibacillosis worldwide. The present study investigated the circulating phylotypes, existence of virulence genes (VGs), and antimicrobial resistance (AMR) in 392 APEC isolates, obtained from 130 samples belonged to six farms using both phenotypic and PCR-based molecular approaches. Congo red binding (CRB) assay confirmed 174 APEC isolates which were segregated into ten, nine, and eight distinct genotypes by RAPD assay (discriminatory index, DI = 0.8707), BOX-PCR (DI = 0.8591) and ERIC-PCR (DI = 0.8371), respectively. The combination of three phylogenetic markers (chuA, yjaA and DNA fragment TspE4.C2) classified APEC isolates into B23 (37.36%), A1 (33.91%), D2 (11.49%), B22 (9.20%), and B1 (8.05%) phylotypes. Majority of the APEC isolates (75–100%) harbored VGs (ial, fimH, crl, papC, and cjrC). These VGs (papC and cjrC) and phylotypes (D2 and B2) of APEC had significant (p = 0.004) association with colibacillosis. Phylogenetic analysis showed two distinct clades (clade A and clade B) of APEC, where clade A had 98–100% similarity with E. coli APEC O78 and E. coli EHEC strains, and clade B had closest relationship with E. coli O169:H41 strain. Interestingly, phylogroups B2 and D2 were found in the APEC strains of both clades, while the strains from phylogroups A1 and B1 were found in clade A only. In this study, 81.71% of the isolates were biofilm formers, and possessed plasmids of varying ranges (1.0 to 54 kb). In vitro antibiogram profiling revealed that 100% isolates were resistant to ≥3 antibiotics, of which 61.96%, 55.24%, 53.85%, 51.16% and 45.58% isolates in phylotypes B1, D2, B22, B23, and A1, respectively, were resistant to these antimicrobials. The resistance patterns varied among different phylotypes, notably in phylotype B22, showing the highest resistance to ampicillin (90.91%), nalidixic acid (90.11%), tetracycline (83.72%), and nitrofurantoin (65.12%). Correspondence analysis also showed significant correlation among phylotypes with CRB (p = 0.008), biofilm formation (p = 0.02), drug resistance (p = 0.03), and VGs (p = 0.06). This report demonstrated that B2 and A1 phylotypes are dominantly circulating APEC phylotypes in Bangladesh; however, B2 and D2 are strongly associated with the pathogenicity. A high prevalence of antibiotic-resistant APEC strains from different phylotypes suggest the use of organic antimicrobial compounds, and/or metals, and the rotational use of antibiotics in poultry farms in Bangladesh.

scholarly journals Multidrug-Resistant Avian Pathogenic Escherichia coli Strains and Association of Their Virulence Genes in Bangladesh

2020 ◽  
Author(s):  
Otun Saha ◽  
M. Nazmul Hoque ◽  
Ovinu Kibria Islam ◽  
Md. Mizanur Rahaman ◽  
Munawar Sultana ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Virulence Genes ◽  
Multidrug Resistant ◽  
Antibiotic Resistant ◽  
E Coli ◽  
Molecular Approaches ◽  
Clade B ◽  
High Prevalence ◽  
Resistance Patterns

AbstractThe avian pathogenic Escherichia coli (APEC) strains are the chief etiology of avian colibacillosis worldwide. The present study investigated the circulating phylotypes, existence of virulence genes (VGs) and antimicrobial resistance (AMR) in 392 APEC isolates, obtained from 130 samples belonged to six farms using both phenotypic and PCR-based molecular approaches. Congo red binding (CRB) assay confirmed 174 APEC isolates which were segregated into 10, 9 and 8 distinctive genotypes by RAPD assay (discriminatory index, D=0.8707), BOX-PCR (D=0.8591) and ERIC-PCR (D=0.8371), respectively. The combination of three phylogenetic markers (chuA, yjaA and DNA fragment TspE4.C2) classified APEC isolates into B23 (37.36%), A1 (33.91%), D2 (11.49%), B22 (9.20%) and B1 (8.05%) phylotypes. Majority of the APEC isolates (75-100%) harbored VGs (ial, fimH, crl, papC and cjrC), and of them, VGs (papC and cjrC) and phylotypes (D2 and B2) of APEC had significant (p=0.004) association with colibacillosis. Phylogenetic analysis showed two distinct clades (Clade A and Clade B) of APEC where Clade A had 98-100.0% similarity with E. coli APEC O78 and E. coli EHEC strains, and Clade B had closest relationship with E. coli O169:H41 strain. Interestingly, phylogroups B2 and D2 were found in the APEC strains of both clades while the strains from phylogroups A1 and B1 were found in clade A only. In this study, 81.71% of the isolates were biofilm formers and possessed plasmids of varying ranges (1.0 to 54 kb). In vitro antibiogram profiling revealed that 100.0% isolates were resistant to ≥3 antibiotics, of which61.96%, 55.24, 53.85, 51.16 and 45.58 % isolates in phylotypes B1, D2, B22, B23 and A1, respectively were these antimicrobials. The resistance patterns varied among different phylotypes, notably in phylotype B22 showing the highest resistance to ampicillin (90.91%), nalidixic acid (90.11%), tetracycline (83.72%) and nitrofurantoin (65.12%). Correspondence analysis also showed significant correlation of phylotypes with CRB (p=0.008), biofilm formation (p=0.02), drug resistance (p=0.03) and VGs (p=0.06). This report demonstrated that B2 and A1 phylotypes are dominantly circulating APEC phylotypes in Bangladesh; however, B2 and D2 are strongly associated with the pathogenicity. A high prevalence of antibiotic resistant APEC strains from different phylotypes suggest to use of organic antimicrobial compounds, and/or metals, and the rotational use of antibiotics in the poultry farms in Bangladesh.

scholarly journals Antibiotic Resistance and Virulence Gene Patterns Associated with Avian Pathogenic Escherichia coli (APEC) from Broiler Chickens in Qatar

Antibiotics ◽  
2021 ◽  
Vol 10 (5) ◽  
pp. 564
Author(s):  
Alreem Johar ◽  
Najlaa Al-Thani ◽  
Sara H. Al-Hadidi ◽  
Elyes Dlissi ◽  
Mahmoud H. Mahmoud ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antibiotic Resistance ◽  
Broiler Chickens ◽  
Virulence Genes ◽  
Virulence Gene ◽  
Avian Pathogenic Escherichia Coli ◽  
E Coli ◽  
Pathogenic Escherichia Coli ◽  
Special Programs ◽  
Resistance Patterns

Avian Pathogenic Escherichia coli (APEC) is the contributing agent behind the avian infectious disease colibacillosis, which causes substantial fatalities in poultry industries that has a significant impact on the economy and food safety. Several virulence genes have been shown to be concomitant with the extraintestinal survival of APEC. This study investigates the antibiotic resistance patterns and APEC-associated virulence genes content in Escherichia coli isolated from non-healthy and healthy broiler chickens from a commercial poultry farm in Qatar. A total of 158 E. coli strains were isolated from 47 chickens from five different organs (air sac, cloacal, kidney, liver, and trachea). Based on genetic criteria, 65% were APEC strains containing five or more virulence genes, and 34% were non-pathogenic E. coli (NPEC) strains. The genes ompT, hlyF, iroN, tsh, vat, iss, cvi/cva, and iucD were significantly prevalent in all APEC strains. E. coli isolates showed 96% resistance to at least one of the 18 antibiotics, with high resistance to ampicillin, cephalothin, ciprofloxacin, tetracycline, and fosfomycin. Our findings indicate high antibiotic resistance prevalence in non-healthy and healthy chicken carcasses. Such resistant E. coli can spread to humans. Hence, special programs are required to monitor the use of antibiotics in chicken production in Qatar.

Serological diversity, molecular characterisation and antimicrobial sensitivity of avian pathogenic Escherichia coli (APEC) isolates from broiler chickens in Kashmir, India

2019 ◽  
Vol 59 (2) ◽  
pp. 338
Author(s):  
S. N. Magray ◽  
S. A. Wani ◽  
Z. A. Kashoo ◽  
M. A. Bhat ◽  
S. Adil ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Broiler Chickens ◽  
Virulence Genes ◽  
Virulence Gene ◽  
Gene Profile ◽  
Avian Pathogenic Escherichia Coli ◽  
Pathogenic Escherichia Coli ◽  
Significant Difference ◽  
Virulence Gene Profile

The present study has determined the serological diversity, virulence-gene profile and in vitro antibiogram of avian pathogenic Escherichia coli (APEC) isolates from broiler chickens in India suspected to have died of colibacillosis. The virulence-gene profile of APEC was compared with that of the Escherichia coli isolates from faeces of apparently healthy chickens, called avian faecal E. coli (AFEC). In total, 90 representative isolates of APEC and 63 isolates of AFEC were investigated in the present study. The APEC were typed into 19 serogroups, while some isolates were rough and could not be typed. Most prevalent serogroup was O2 (24.44%). Among the eight virulence genes studied, the prevalence of seven genes (iss, iucD, tsh, cva/cvi, irp2, papC and vat) was significantly higher in APEC than in AFEC isolates. However, there was no significant difference between APEC and AFEC isolates for possession of astA gene. The most frequent gene detected among the two groups of organisms was iss, which was present in 98.88% and 44.44% of APEC and AFEC isolates respectively. The in vitro antibiogram showed that the majority (96.6%) of APEC isolates were resistant to tetracycline, while 82.2% were resistant to cephalexin, 78.8% to cotrimoxazole, 68.8% to streptomycin and 63.3% to ampicillin. However, most of them (84.45%) were sensitive to gentamicin. Thus, it is concluded that APEC from the broiler chickens carried putative virulence genes that attributed to their pathogenicity. Furthermore, the majority of APEC isolates were found to be multi-drug resistant, which, in addition to leading treatment failures in poultry, poses a public health threat.

scholarly journals Molecular Detection of Avian Pathogenic Escherichia coli (APEC) for the First Time in Layer Farms in Bangladesh and Their Antibiotic Resistance Patterns

2020 ◽  
Vol 8 (7) ◽  
pp. 1021 ◽  
Author(s):  
Samina Ievy ◽  
Md. Saiful Islam ◽  
Md. Abdus Sobur ◽  
Mithun Talukder ◽  
Md. Bahanur Rahman ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antibiotic Resistance ◽  
Virulence Genes ◽  
Molecular Detection ◽  
Avian Pathogenic Escherichia Coli ◽  
Internal Organs ◽  
Pathogenic Escherichia Coli ◽  
Resistance Patterns ◽  
Antibiotic Resistance Patterns ◽  
First Time

Avian pathogenic Escherichia coli (APEC) causes significant economic losses in poultry industries. Here, we determined for the first time in Bangladesh, the prevalence of APEC-associated virulence genes in E. coli isolated from layer farms and their antibiotic resistance patterns. A total of 99 samples comprising internal organs, feces, and air were collected from 32 layer farms. Isolation was performed by culturing samples on eosin–methylene blue agar plates, while the molecular detection of APEC was performed by PCR, and antibiograms were performed by disk diffusion. Among the samples, 36 were positive for the APEC-associated virulence genes fimC, iucD, and papC. Out of 36 isolates, 7, 18, and 11 were positive, respectively, for three virulence genes (papC, fimC, and iucD), two virulence genes, and a single virulence gene. Although the detection of virulence genes was significantly higher in the internal organs, the air and feces were also positive. The antibiograms revealed that all the isolates (100%) were resistant to ampicillin and tetracycline; 97.2%, to chloramphenicol and erythromycin; 55.5%, to enrofloxacin; 50.0%, to norfloxacin and ciprofloxacin; 19.4%, to streptomycin; 11.1%, to colistin; and 8.33%, to gentamicin. Interestingly, all the isolates were multidrug-resistant (MDR). Spearman’s rank correlation coefficient analysis revealed the strongest significant correlation between norfloxacin and ciprofloxacin resistance. This is the first study in Bangladesh describing the molecular detection of APEC in layer farms. Isolated APEC can now be used for detailed genetic characterization and assessing the impact on public health.

scholarly journals Complete DNA Sequence of a ColBM Plasmid from Avian Pathogenic Escherichia coli Suggests that It Evolved from Closely Related ColV Virulence Plasmids

2006 ◽  
Vol 188 (16) ◽  
pp. 5975-5983 ◽  
Author(s):  
Timothy J. Johnson ◽  
Sara J. Johnson ◽  
Lisa K. Nolan
Keyword(s):  
Escherichia Coli ◽  
Southern Blotting ◽  
Virulence Genes ◽  
Complete Sequence ◽  
Economic Losses ◽  
Avian Pathogenic Escherichia Coli ◽  
Prevalence Studies ◽  
E Coli ◽  
Virulence Plasmids ◽  
Pathogenic Escherichia Coli

ABSTRACT Avian pathogenic Escherichia coli (APEC), an extraintestinal pathogenic E. coli causing colibacillosis in birds, is responsible for significant economic losses for the poultry industry. Recently, we reported that the APEC pathotype was characterized by possession of a set of genes contained within a 94-kb cluster linked to a ColV plasmid, pAPEC-O2-ColV. These included sitABCD, genes of the aerobactin operon, hlyF, iss, genes of the salmochelin operon, and the 5′ end of cvaB of the ColV operon. However, the results of gene prevalence studies performed among APEC isolates revealed that these traits were not always linked to ColV plasmids. Here, we present the complete sequence of a 174-kb plasmid, pAPEC-O1-ColBM, which contains a putative virulence cluster similar to that of pAPEC-O2-ColV. These two F-type plasmids share remarkable similarity, except that they encode the production of different colicins; pAPEC-O2-ColV contains an intact ColV operon, and pAPEC-O1-ColBM encodes the colicins B and M. Interestingly, remnants of the ColV operon exist in pAPEC-O1-ColBM, hinting that ColBM-type plasmids may have evolved from ColV plasmids. Among APEC isolates, the prevalence of ColBM sequences helps account for the previously observed differences in prevalence between genes of the “conserved” portion of the putative virulence cluster of pAPEC-O2-ColV and those genes within its “variable” portion. These results, in conjunction with Southern blotting and probing of representative ColBM-positive strains, indicate that this “conserved” cluster of putative virulence genes is primarily linked to F-type virulence plasmids among the APEC isolates studied.

scholarly journals Virulence gene profiles of avian pathogenic Escherichia coli isolated from chickens with colibacillosis in Bulawayo, Zimbabwe

2015 ◽  
Vol 82 (1) ◽  
Author(s):  
Joshua Mbanga ◽  
Yvonne O. Nyararai
Keyword(s):  
Escherichia Coli ◽  
Virulence Genes ◽  
Virulence Gene ◽  
Economic Losses ◽  
Avian Pathogenic Escherichia Coli ◽  
Pcr Assay ◽  
E Coli ◽  
Gene Profiles ◽  
Pathogenic Escherichia Coli ◽  
Polymerase Chain

Colibacillosis, a disease caused by avian pathogenic Escherichia coli (APEC), is one of the main causes of economic losses in the poultry industry worldwide. This study was carried out in order to determine the APEC-associated virulence genes contained by E. coli isolates causing colibacillosis in chickens. A total of 45 E. coli isolates were obtained from the diagnostics and research branch of the Central Veterinary Laboratories, Bulawayo, Zimbabwe. These isolates were obtained from chickens with confirmed cases of colibacillosis after postmortem examination. The presence of the iutA, hlyF, ompT, frz, sitD, fimH, kpsM, sitA, sopB, uvrY, pstB and vat genes were investigated by multiplex polymerase chain reaction (PCR) assay. Of the 45 isolates, 93% were positive for the presence of at least one virulence gene. The three most prevalent virulence genes were iutA (80%), fimH (33.3%) and hlyF (24.4%). The kpsM, pstB and ompT genes had the lowest prevalence, having been detected in only 2.2% of the isolates. All 12 virulence genes studied were detected in the 45 APEC isolates. Virulence gene profiles were constructed for each APEC isolate from the multiplex data. The APEC isolates were profiled as 62.2% fitting profile A, 31.1% profile B and 6.7% profile C. None of the isolates had more than seven virulence genes. Virulence profiles of Zimbabwean APEC isolates are different from those previously reported. Zimbabwean APEC isolates appear to be less pathogenic and may rely on environmental factors and stress in hosts to establish infection.

scholarly journals Characterization and antimicrobial resistance patterns of Escherichia coli isolated from feces of healthy broiler chickens

2016 ◽  
Vol 83 (0) ◽  
Author(s):  
Ariel Eurides Stella ◽  
Maria Cristina De Oliveira ◽  
Vera Lúcia Dias da Silva Fontana ◽  
Renato Paris Maluta ◽  
Clarissa Araújo Borges ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Broiler Chickens ◽  
Clinical Signs ◽  
Avian Pathogenic Escherichia Coli ◽  
E Coli ◽  
The Past ◽  
Pathogenic Escherichia Coli ◽  
Resistance Patterns ◽  
Resistant Strains ◽  
Polymerase Chain

ABSTRACT: Avian pathogenic Escherichia coli (APEC) strains are isolated from lesions of poultry presenting colibacillosis, which is a disease that causes either systemic or localized clinical signs. Such strains share many characteristics with E. coli strains that cause extra-intestinal illness in humans. There is not a consensus on how to define the APEC pathotype with regard to the presence of virulence traits. On the other hand, in the past few years, five minimal predictors for APEC detection were proposed. The E. coli isolates in this work were tested through polymerase chain reaction (PCR) to the five proposed minimal predictors and cva C. The strains presenting them were categorized as potential APEC. The APEC and non-APEC categories showed high resistance (> 50%) to cephalotin, erythromycin, streptomycin, sulphametoxazol/trimethoprim, ampicillin, and amoxicillin. Potential APEC strains were significantly more resistant to cephalotin (p < 0.05) and neomcycin (p < 0.01) than non-APEC. These latter were significantly more resistant to tetracycline (p < 0.01) than the potential APEC strains. These results demonstrate that feces of poultry present E. coli strains with resistant features, showing or not the potential of causing colibacillosis in poultry. Because APEC and extra-intestinal illness in humans may be similar, these resistant strains are of interest to public health.

IDENTIFICATION OF THE AVIAN PATHOTYPE OF ESCHERICHIA COLI ON LAYER FLOCKS BY MULTIPLEX PCR

2019 ◽  
Vol 7 ◽  
pp. 905-911
Author(s):  
Marilena Burtan ◽  
Virgilia Popa ◽  
Maria Rodica Gurau ◽  
Doina Danes
Keyword(s):  
Escherichia Coli ◽  
Multiplex Pcr ◽  
Virulence Genes ◽  
Virulence Gene ◽  
Economic Losses ◽  
Ompa Gene ◽  
Avian Pathogenic Escherichia Coli ◽  
E Coli ◽  
Pathogenic Escherichia Coli

Introduction: Colibacillosis in poultry is determined by avian pathogenic Escherichia coli (APEC) and represents an important source of economic losses  in the poultry industry. APEC’s pathogenicity relies on the presence and expression of different virulence factors. The genes ompA , iss  and  fimH, encoding the outer membrane protein, the protein inducing resistance to complement and the synthesis of type 1 fimbria are present in APEC strains. Objective: Escherichia coli strains isolated from layers were analysed to assess the pathotype they belong to. Methods: In order to detect the three genes associated with APEC strains, 16 E. coli isolates were investigated for virulence associated genes ompA, iss and fimH, using multiplex PCR. Results: From the 16 E.coli strains submitted, multiplex PCR assessment revealed that 14 (87.5%) of the E. coli strains isolated contained at least one virulence gene, while 2 (12.5%) strains did not harbour any of the virulence genes tested. The fimH gene was noted in 13 (81.25%) of the strains tested, the ompA gene has been present in 12 (75%) strains and the iss gene was present in 9 (56.25%) strains. Eight (50%) strains were found to present all three investigated genes. Conclusion: Presence of these genes is a strong indicatory to consider those strains as belonging to the APEC pathotype.

scholarly journals Antibiotic Resistance and Virulence Gene Patterns Associated with Avian Pathogenic Escherichia coli from Broiler Chickens in Qatar

2021 ◽  
Author(s):  
Alreem Johar ◽  
Najlaa Al-Thani ◽  
Sara Al-Hadidi ◽  
Elyes Dlissi ◽  
Mahmoud Mahoud ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antibiotic Resistance ◽  
Broiler Chickens ◽  
Virulence Genes ◽  
Virulence Gene ◽  
Avian Pathogenic Escherichia Coli ◽  
Chi Square ◽  
E Coli ◽  
Pathogenic Escherichia Coli ◽  
Special Programs

Introduction: Avian Pathogenic Escherichia coli (APEC) is the contributing agent behind the avian infectious disease colibacillosis, which causes substantial fatalities in poultry industries that significantly impact the economy and food safety. Several virulence genes have been shown to be concomitant with the extra-intestinal survival of APEC. This study investigates the antibiotic resistance patterns and APEC‐associated virulence genes content in Escherichia coli (E. coli) isolated from non‐healthy and healthy broiler chickens from a commercial poultry farm in Qatar. Material and Methods: 158 E. coli strains were isolated from 47 chickens from five different organs (air sac, cloacal, kidney, liver, and trachea). Genomic DNA was extracted from E. coli using the QIAamp Pathogen Mini Kit. Multiplex PCR was executed to detect tsh, iucD, ompT, hlyF, iroN, iss, vat, cvi/cva genes associated with PPEC. Antibiotic susceptibility testing was performed using the standard Kirby-Bauer disk and E-test. Amplified virulence genes detected were sequenced and analyzed. Graph Pad version 8 and PAST software version 4.03 were used for statistical and clustering analysis. The chi-square test was performed on all data to compare the antibiotic resistance and virulence gene patterns between non-healthy and healthy chicken samples Results: 65% of the isolated bacteria were APEC strains containing five or more virulence genes, and 34% were non‐pathogenic E. coli (NPEC) strains. The genes ompT, hlyF, iroN, tsh, vat, iss, cvi/cva, and iucD were significantly prevalent in all APEC strains. E. coli isolates showed 96% resistance to at least one of the 18 antibiotics, with high resistance to ampicillin, cephalothin, ciprofloxacin, tetracycline, and fosfomycin. Conclusions: Our findings indicate high antibiotic resistance prevalence in non-healthy and healthy chicken carcasses. Such resistant E. coli can spread to humans. Hence, special programs are required to monitor the use of antibiotics in chicken production in Qatar.

scholarly journals Molecular profile of avian pathogenic Escherichia coli (APEC) from poultry associated with colibacillosis in Algeria

2020 ◽  
Vol 71 (2) ◽  
pp. 2113
Author(s):  
M. LOUNIS ◽  
G. ZHAO ◽  
Y. LI ◽  
Y. GAO ◽  
J. WANG ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Virulence Genes ◽  
Molecular Profile ◽  
Avian Pathogenic Escherichia Coli ◽  
Highly Pathogenic ◽  
E Coli ◽  
Pathogenic Escherichia Coli ◽  
Six Genes

The objective of the present study was the detection of virulence-associated genes of E. coli isolated from chicken with colibacillosis. Seventeen (17) APEC isolates were examined by two panels of PCRs for the presence of 11 genes described for avian pathogenic (hlyF, iroN, iss, ompT, iutA and fimC) and diarrheagenic (eae, stx, est, elt, ipaH and aggR) E. coli. Results revealed that none of the APEC isolates harbored the genes eae, stx, est, elt, ipaH and aggR. In another hand, 88.2% of the isolates were positive for 3 or more of the virulence genes hlyF, iroN, iss, ompT, iutA and fimC. Also, 35.3% of the isolates harbored all the six genes. Genes fimC (88.2%), iss (82.3%) and ompT (76.5%) were the most prevalent while genes hylF, iutA and iroN which were present with the same frequency (52.9%) were mostly associated with highly pathogenic strains. 

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