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Antimicrobial Resistance, Virulence Factor-Encoding Genes, and Biofilm-Forming Ability of Community-Associated Uropathogenic Escherichia coli in Western Saudi Arabia

Sara H. Arafa
Sara H. Arafa
, 
Wafa A. Alshehri
Wafa A. Alshehri
, 
Sameer R. Organji
Sameer R. Organji
, 
Khaled Elbanna
Khaled Elbanna
, 
Najla A. Obaid
Najla A. Obaid
, 
Mohammad S. Aldosari
Mohammad S. Aldosari
, 
Fatimah H. Asiri
Fatimah H. Asiri
, 
Iqbal Ahmad
Iqbal Ahmad
 und 
Hussein H. Abulreesh
Hussein H. Abulreesh
   | 02. Sept. 2022
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Article Category: Original Paper
Online veröffentlicht: 02. Sept. 2022
Seitenbereich: 325 - 339
Eingereicht: 27. Apr. 2022
Akzeptiert: 01. Juli 2022
DOI: https://doi.org/10.33073/pjm-2022-029
Schlüsselwörter
© 2022 Sara H. Arafa et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1A

Agarose gel electrophoresis shows positive results of kpsMTII virulence gene at (270 bp) in UPEC. M– DNA marker, C– negative control
Agarose gel electrophoresis shows positive results of kpsMTII virulence gene at (270 bp) in UPEC. M– DNA marker, C– negative control

Fig. 1B

Agarose gel electrophoresis shows positive results of csgA virulence gene at (301 bp) in UPEC. M– DNA marker, C– negative control
Agarose gel electrophoresis shows positive results of csgA virulence gene at (301 bp) in UPEC. M– DNA marker, C– negative control

Fig. 1C

Agarose gel electrophoresis shows some positive results of vat virulence gene at (418 bp) in UPEC. M– DNA marker, C– negative control
Agarose gel electrophoresis shows some positive results of vat virulence gene at (418 bp) in UPEC. M– DNA marker, C– negative control

Multidrug-resistance patterns among uropathogenic E. coli.

Isolate code Origin Antibiotic resistance patterns No. of antimicrobial classes ESBL† KPC‡
** UPEC 2 F AM, CEFT, CEFE, TS 3 – –
** UPEC 6 F AM, CEFT, CEFE, CIP, NOR, TS 4 + +
** UPEC 12 F AM, CEFT, CEFE, CIP, NOR, TS 4 + +
** UPEC 13 F AM, CEFT, CEFE, CIP, NOR, TS 4 + +
** UPEC 17 M AM, CEFT, CEFE, CIP, TS 4 – –
UPEC 20 F NOR 1 – –
** UPEC 25 F AM, AC, PT*, CIP, NOR, NIT* 3 – –
** UPEC 32 F AM, CEFT, CEFE, CIP, NOR, TS 4 + +
** UPEC 39 M AM, CEFT, CEFE, NIT 3 + +
** UPEC 45 M AM, CEFT, CEFE, CIP, NOR, TS 4 + +
UPEC 88 F AM, NOR 2 – –
** UPEC 95 F AM, CEFT, CEFE, NOR, TS 4 + +
** UPEC 119 F AM, CEFT, CEFE, NOR 3 + +
UPEC 127 M NOR 1 – –
UPEC 138 F NOR 1 – –
UPEC 145 F NOR 1 – –
UPEC 151 F NOR 1 – –
UPEC 156 M NOR 1 – –
UPEC 168 F NOR 1 – –
** UPEC 192 M AM, CEFT, CEFE, NOR, TS 4 + +
** UPEC 213 M AM, CEFT, CEFE, CIP, NOR, TS 4 + +
** UPEC 225 M AM, G, CIP, NOR, TS 4 – –
UPEC 226 M NOR 1 – –
UPEC 230 M NOR 1 – –
UPEC 242 M NOR 1 – –
** UPEC 243 F AM, G, CIP, NOR, TS, NIT* 4 – –
** UPEC 316 F AM, CEFT, CEFE, G, CIP, NOR, TS 5 + +
** UPEC 326 F AM, CEFT, CEFE, G, CIP, NOR, TS 5 + +
UPEC 331 M NOR 1 – –
** UPEC 353 F AM, CEFT, CEFE, TS 3 + –
** UPEC 425 M AM, AC, PT, NOR, TS 3 – –
UPEC 432 M NOR 1 – –
** UPEC 450 M AM, AC*, CEFT, CEFE, G, CIP, NOR, TS 5 + +
** UPEC 544 F AM, AC*, G, NOR, TS 4 – –
** UPEC 549 M AM, CEFT, CEFE, CIP, TS 4 + +
** UPEC 661 F AM, CEFT, CEFE, TS 3 + +
UPEC 662 F AM 1 – –
UPEC 666 F AM, CEFT, CEFE 2 + +
UPEC 738 M AM 1 – –
UPEC 829 F AM, TS 2 – –
UPEC 950 M AM, TS 2 – –
UPEC 1000 M AM, NIT 2 + +

Prevalence of ESBL, KPC and α-hemolysin positive phenotypes of UPEC.

Isolates origin Total number of UPEC ESBL+† (%) ESBL+‡ (%) KPC+ (%) β-hemolysis (%)
Male 22   7 (32)   7 (32)   7 (32) 11 (50)
Female 28 11 (39.3) 11 (39.3) 10 (36) 16 (57.2)
Total 50 18 (36) 18 (36) 17 (34) 27 (54)

Calculations of Biofilm classification values.

Biofilm formation ability Range Negative control
Strong (S) Moderate (M) Weak (W)
BF = AB– CW ≥ 0.200 – 0.299 0.100 – 0.199 < 0.100 < 0.100
BF = AB ÷ CW 4.00 – 5.99 2.00 – 3.99 < 2.00 – 1.00 < 1.00

Semiquantitative classification of biofilm formation using two different formulas and the association of biofilm-forming ability and multidrug-resistance in uropathogenic E. coli.

Isolate code BF† BF‡ AMR
UPEC (2) N (0.058) W (1.167) 3
UPEC (6) M (0.185) N (0.420) 4
UPEC (12) S (0.343) W (1.988) 4
UPEC (13) S (0.365) M (2.051) 4
UPEC (17) N (0.066) W (1.190) 4
UPEC (20) S (0.313) W (1.902) 1
UPEC (25) M (0.121) W (1.348) 2
UPEC (32) N (0.067) W (1.193) 4
UPEC (39) W (0.39) M (2.123) 2
UPEC (45) N (0.086) W (1.247) 4
UPEC (88) N (0.066) W (1.190) 2
UPEC (95) N (0.086) W (1.247) 4
UPEC (119) N (0.046) W (1.132) 4
UPEC (127) S (0.339) W (1.976) 1
UPEC (138) S (0.239) W (1.688) 1
UPEC (145) M (0.151) W (1.435) 1
UPEC (151) M (0.135) W (1.389) 1
UPEC (156) W (0.057) W (1.164) 1
UPEC (168) W (0.031) W (1.089) 1
UPEC (192) W (0.034) W (1.097) 4
UPEC (213) W (0.074) W (1.213) 4
UPEC (225) M (0.187) W (1.538) 4
UPEC (226) M (0.121) W (1.348) 1
UPEC (230) N (0.068) W (1.178) 1
UPEC (242) N (–0.015) N (0.960) 1
UPEC (243) N (0.062) W (1.162) 4
UPEC (316) N (0.016) W (1.041) 5
UPEC (326) N (–0.027) N (0.929) 5
UPEC (331) N (0.004) W (1.010) 1
UPEC (353) N (0.031) W (1.081) 3
UPEC (425) N (–0.017) N (0.955) 3
UPEC (432) N (0.027) W (1.070) 1
UPEC (450) N (0.054) W (1.141) 5
UPEC (544) N (0.061) W (1.159) 4
UPEC (549) S (0.216) W (1.565) 4
UPEC (601) N (0.024) W (1.062) 0
UPEC (654) N (0.013) W (1.034) 0
UPEC (661) N (0.088) W (1.230) 3
UPEC (662) M (0.125) W (1.327) 1
UPEC (666) N (0.068) W (1.178) 2
UPEC (704) S (0.328) W (1.858) 0
UPEC (738) N (–0.017) N (0.955) 1
UPEC (829) N (–0.027) N (0.929) 2
UPEC (842) N (0.074) W (1.193) 0
UPEC (848) S (0.379) W (1.992) 0
UPEC (882) N (0.09) W (1.235) 0
UPEC (900) N (0.068) W (1.190) 0
UPEC (928) N (0.074) W (1.193) 0
UPEC (950) M (0.121) W (1.348) 2
UPEC (1000) M (0.121) W(1.338) 2
r –0.0948 –0.1475 NS

The sequence, annealing temperatures and the product size of the primers used to amplify genes encoding virulence factors and antimicrobial resistance.

Gene/ primer Sequence Product size (bp) Annealing temperature
kps MTII FP: 5'–GCGCATTTGCTGATACTGTTG-3'RP: 5'–CATCCAGACGATAAGCATGAGCA-3' 270 62
traT FP: 5'–GGTGTGGTGCGATGAGCACAG-3'RP: 5'–CACGGTTCAGCCATCCCTGAG-3' 288 62
sat FP: 5'–TCAGAAGCTCAGCGAATCATTG-3'RP: 5'–CCATTATCACCAGTAAAACGCACC-3' 931 59
csgA FP: 5'–GGCGGAAATGGTTCAGATGTTG-3'RP: 5'–CGTATTCATAAGCTTCTCCCGA-3' 301 60
vat FP: 5'–AACGGTTGGTGGCAACAATCC-3'RP: 5'–AGCCCTGTAGAATGGCGAGTA-3' 418 58
iutA FP: 5'–GGCTGGACATCATGGGAACTGG-3'RP: 5'–CGTCGGGAACGGGTAGAATCG-3' 302 85
blaKPC FP: 5'–GATACCACGTTCCGTCTGG-3'RP: 5'–GCAGGTTCCGGTTTTGTCTC-3' 246 50-60
blaCTX-M FP: 5'–TTTGCGATGTGCAGTACCAGTAA-3'RP: 5'–CGATATCGTTGGTGGTGCCATA-3' 544 62

Antimicrobial resistance (Intermediate resistance*) profiles of uropathogenic E. coli in western Saudi Arabia.

Sample origin N P (%) AM AC PT CEFT CEFE ERT IMI MER AMI G CIP NOR NIT TS
Male 774 22 (2.84) 12 1, (1*) 1 7 7 0 0 0 0 2 6 19 2 9
Female 226 28 (12.4) 18 1, (1*) (1*) 12 12 0 0 0 0 4 8 22 (2*) 13
Total 1,000 50 (5) 30 4 2 19 19 0 0 0 0 6 14 41 4 22
p < 0.001

Prevalence of genes encoding virulence factors and antimicrobial resistance in uropathogenic E. coli.

Isolates origin Total number of UPEC Genes encoding for virulence factors
kpsMTII (%) iutA (%) traT (%) csgA (%) Sat (%) Vat (%)
Male 22 22 (100) 22 (100) 22 (100) 22 (100) 22 (100)   9 (41)
Female 28 28 (100) 28 (100) 28 (100) 28 (100) 27 (97) 10 (36)
Total 50 50 (100) 50 (100) 50 (100) 50 (100) 49 (98) 19 (38)
Genes encoding for antimicrobial resistance
blaCTX-M (%) blaKPC (%)
Male 22   8 (37)   7 (32)
Female 28 10 (36)   5 (18)
Total 50 18 (36) 12 (24)
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