Antibiotic resistance, phylogenetic typing, and virulence genes profile analysis of uropathogenic Escherichia coli isolated from patients in southern Iraq.
Antibiotic resistance
Phylogenetic groups
Uropathogenic Escherichia coli
Virulence factor genes
Journal
Journal of applied genetics
ISSN: 2190-3883
Titre abrégé: J Appl Genet
Pays: England
ID NLM: 9514582
Informations de publication
Date de publication:
May 2022
May 2022
Historique:
received:
06
04
2021
accepted:
12
01
2022
revised:
17
10
2021
pubmed:
11
2
2022
medline:
7
4
2022
entrez:
10
2
2022
Statut:
ppublish
Résumé
Of the most common infectious diseases that occur mainly by uropathogenic Escherichia coli (UPEC) is urinary tract infections (UTIs). The purpose of this study was to investigate virulence factors, antibiotic resistance, and phylogenetic groups among UPEC strains isolated from patients with UTI in southern Iraq. A total of 100 UPEC isolates were collected from urine samples of UTI patients from various hospitals in southern Iraq, and confirmed by morphological and biochemical tests. Antimicrobial susceptibility testing on isolates was performed by disk diffusion method. Multiplex PCR techniques were used to evaluate the phylogenetic groups based on Clermont method and to detect the presence of six virulence factor genes. The majority of isolates belonged to the phylogenetic groups B2 (46%) and C (13%). The most prevalent virulence factors were fimH (96%), followed by aer (47%), papC (36%), cnf1 (17%), hly (15%), and afa (8%). Phenotypic testing showed that the isolates were most resistant to piperacillin, ticarcillin, amoxicillin/clavulanic acid (92%, 91%, and 88%, respectively) and most sensitive to amikacin and imipenem, respectively. The maximum antibiotic resistance and virulence factors were observed in the phylogenetic group B2. The results showed that the UPEC isolates had all six virulence factors with high frequency and the highest drug resistance. Besides, the results showed a direct relationship between virulence factors, gene diversity, phylogenetic background, and antimicrobial resistance in the UPEC isolates.
Identifiants
pubmed: 35143031
doi: 10.1007/s13353-022-00683-2
pii: 10.1007/s13353-022-00683-2
doi:
Substances chimiques
Anti-Bacterial Agents
0
Virulence Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
401-412Subventions
Organisme : Ferdowsi University of Mashhad
ID : 3/46008
Informations de copyright
© 2022. The Author(s), under exclusive licence to Institute of Plant Genetics Polish Academy of Sciences.
Références
AbdALameer R (2015) Genotyping of Escherichia coli isolated from clinical and hospitals environment. Univ Thi-Qar J Sci 5:3–13
Ahmed N, Zeshan B, Naveed M, Afzal M, Mohamed M (2019) Antibiotic resistance profile in relation to virulence genes fimH, hlyA and usp of uropathogenic E. coli isolates in Lahore, Pakistan. Trop Biomed 36:559–568
pubmed: 33597418
Al-Gasha’a FA, Al-Baker SM, Obiad JM, Alrobiai FA (2020) Prevalence of urinary tract infections and associated risk factors among patients attending medical city hospital in Baghdad City, Iraq. Am J Infect Dis 16(2):77–84. https://doi.org/10.3844/ajidsp.2020.77.84
doi: 10.3844/ajidsp.2020.77.84
Ali Abdi H, Rashki Ghalehnoo M (2015) Virulence genes, genetic diversity, antimicrobial susceptibility and phylogenetic background of Escherichia coli isolates. Int J Enteric Pathog 3(3):1–7. https://doi.org/10.17795/ijep25692
doi: 10.17795/ijep25692
Al-Naqshbandi AA, Chawsheen MA, Abdulqader HH (2019) Prevalence and antimicrobial susceptibility of bacterial pathogens isolated from urine specimens received in rizgary hospital—Erbil. J Infect Public Health 12:330–336. https://doi.org/10.1016/j.jiph.2018.11.005
doi: 10.1016/j.jiph.2018.11.005
pubmed: 30522892
Ballesteros-Monrreal MG, Arenas-Hernández MMP, Enciso-Martínez Y, Martínez-de la Peña CF, Rocha-Gracia RC, Lozano-Zaraín P, Navarro-Ocaña A, Martínez-Laguna Y, de la Rosa-López R (2020) Virulence and resistance determinants of uropathogenic Escherichia coli strains isolated from pregnant and non-pregnant women from two states in Mexico. Infect Drug Resist 13:295–310. https://doi.org/10.2147/IDR.S226215
doi: 10.2147/IDR.S226215
pubmed: 32099421
pmcid: 6997036
Boroumand M, Naghmachi M, Ghatee MA (2021) Detection of phylogenetic groups and drug resistance genes of Escherichia coli causing urinary tract infection in Southwest Iran. Jundishapur J Microbiol 14:2. https://doi.org/10.5812/jjm.112547
doi: 10.5812/jjm.112547
Brennan DE, Dowd C, O’Morain C, McNamara D, Smith SM (2018) Can bacterial virulence factors predict antibiotic resistant Helicobacter pylori infection? World J Gastroenterol 24(9):971. https://doi.org/10.3748/wjg.v24.i9.971
doi: 10.3748/wjg.v24.i9.971
pubmed: 29531461
pmcid: 5840472
Cepas V, Soto SM (2020) Relationship between virulence and resistance among gram-negative bacteria. Antibiotics 9(10):719. https://doi.org/10.3390/antibiotics9100719
doi: 10.3390/antibiotics9100719
pmcid: 7589547
Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66(10):4555–4558. https://doi.org/10.1128/aem.66.10.4555-4558.2000
doi: 10.1128/aem.66.10.4555-4558.2000
pubmed: 11010916
pmcid: 92342
Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5(1):58–65. https://doi.org/10.1111/1758-2229.12019
doi: 10.1111/1758-2229.12019
pubmed: 23757131
Da Silva GJ, Mendonça N (2012) Association between antimicrobial resistance and virulence in Escherichia coli. Virulence 3(1):18–28. https://doi.org/10.4161/viru.3.1.18382
doi: 10.4161/viru.3.1.18382
pubmed: 22286707
Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W (2020) Distribution of virulence genes and phylogenetics of uropathogenic Escherichia coli among urinary tract infection patients in Addis Ababa
Demirci M, Ünlü Ö, Tosun Aİ (2019) Detection of O25b-ST131 clone, CTX-M-1 and CTX-M-15 genes via real-time PCR in Escherichia coli strains in patients with UTIs obtained from a university hospital in Istanbul. J Infect Public Health 12(5):640–644. https://doi.org/10.1016/j.jiph.2019.02.017
doi: 10.1016/j.jiph.2019.02.017
pubmed: 30826300
Dobrindt U, Blum-Oehler G, Hartsch T, Gottschalk G, Ron EZ, Fünfstück R, Hacker J (2001) S-Fimbria-encoding determinant sfa I is located on pathogenicity island III536 of uropathogenic Escherichia coli strain 536. Infect Immun 69:4248–4256. https://doi.org/10.1128/IAI.69.7.4248-4256.2001
doi: 10.1128/IAI.69.7.4248-4256.2001
pubmed: 11401961
pmcid: 98494
Ejrnæs K (2011) Bacterial characteristics of importance for recurrent urinary tract infections caused by Escherichia coli. Dan Med Bull 58(2011):B4187
pubmed: 21466767
Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13:269–284. https://doi.org/10.1038/nrmicro3432
doi: 10.1038/nrmicro3432
pubmed: 25853778
pmcid: 4457377
Gordon DM, Clermont O, Tolley H, Denamur E (2008) Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 10:2484–2496. https://doi.org/10.1111/j.1462-2920.2008.01669.x
doi: 10.1111/j.1462-2920.2008.01669.x
pubmed: 18518895
Hadifar S, Moghoofei M, Nematollahi S, Ramazanzadeh R, Sedighi M, Salehi-Abargouei A, Miri A (2016) Epidemiology of multi drug resistant uropathogenic Escherichia coli in Iran: a systematic review and meta-analysis. Jpn J Infect Dis 70(2016):19–25. https://doi.org/10.7883/yoken.JJID.2015.652
doi: 10.7883/yoken.JJID.2015.652
pubmed: 27000462
Hozzari A, Behzadi P, Khiabani PK, Sholeh M, Sabokroo N (2020) Clinical cases, drug resistance, and virulence genes profiling in uropathogenic Escherichia coli. J Appl Genet 1–9
Jalali HR, Pourbakhsh A, Fallah F, Eslami G (2015) Genotyping of virulence factors of uropathogenic Escherichia coli by PCR. Nov Biomed 3:177–181
Johnson JR, Kuskowski MA, O’bryan TT, Colodner R, Raz R, (2005) Virulence genotype and phylogenetic origin in relation to antibiotic resistance profile among Escherichia coli urine sample isolates from Israeli women with acute uncomplicated cystitis. Antimicrob Agents Chemother 49:26–31. https://doi.org/10.1128/AAC.49.1.26-31.2005
doi: 10.1128/AAC.49.1.26-31.2005
pubmed: 15616271
pmcid: 538882
Kaper JB, Nataro JP, Mobley HLT (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 4:123–140. https://doi.org/10.1038/nrmicro818
doi: 10.1038/nrmicro818
Katongole P, Kisawuzi DB, Bbosa HK, Kateete DP, Najjuka CF (2019) Phylogenetic groups and antimicrobial susceptibility patterns of uropathogenic Escherichia coli clinical isolates from patients at Mulago National Referral Hospital, Kampala, Uganda. F1000Research 8(1828):1828
Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, Koo SH, Oh MH, Kim HJ, Choi CH (2016) Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett Appl Microbiol 62:84–90. https://doi.org/10.1111/lam.12517
doi: 10.1111/lam.12517
pubmed: 26518617
Langermann S, Mӧllby R, Burlein JE, Palaszynski SR, Auguste G, DeFusco A, Strouse R, Schenerman MA, Hultgren SJ, Pinkner JS, Winberg J, Guldevall L, Mats Sӧderhäll M, Ishikawa K, Normark S, Koenig S (2000) (2000) Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J Infect Dis 181:774–778
doi: 10.1086/315258
Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J, Barren P, Koenig S, Leath S, Jones H, Hultgren SJ (1997) Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276:607–661
doi: 10.1126/science.276.5312.607
López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, Moncada-Barrón D, Villanueva-Recillas S, Xicohtencatl-Cortes J, Hernández-Castro R (2014) Identification of virulence factors genes in Escherichia coli isolates from women with urinary tract infection in Mexico. Biomed Res Int 2014:959206. https://doi.org/10.1155/2014/959206
doi: 10.1155/2014/959206
pubmed: 24895634
pmcid: 4026957
Miranda-Estrada LI, Ruíz-Rosas M, Molina-López J, Parra-Rojas I, González-Villalobos E, Castro-Alarcón N (2017) Relationship between virulence factors, resistance to antibiotics and phylogenetic groups of uropathogenic Escherichia coli in two locations in Mexico. Enferm Infecc Microbiol Clin 35:426–433. https://doi.org/10.1016/j.eimc.2016.02.021
doi: 10.1016/j.eimc.2016.02.021
pubmed: 27048964
Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, Hultgren SJ (1998) Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282(5393):1494–1497. https://doi.org/10.1126/science.282.5393.1494
doi: 10.1126/science.282.5393.1494
pubmed: 9822381
Müştak HK, Günaydin E, Kaya İB, Salar MÖ, Babacan O, Önat K, … Diker KS (2015) Phylo-typing of clinical Escherichia coli isolates originating from bovine mastitis and canine pyometra and urinary tract infection by means of quadruplex PCR. Vet Q 35(4):194–199
Noie Oskouie A, Hasani A, Ahangarzadeh Rezaee M, Soroush Bar Haghi MH, Hasani A, Soltani E (2019) A relationship between o-serotype, antibiotic susceptibility and biofilm formation in uropathogenic Escherichia coli. Microb Drug Resist 25:951–958. https://doi.org/10.1089/mdr.2018.0330
doi: 10.1089/mdr.2018.0330
pubmed: 30817229
Ørskov I, Ørskov F (1985) Escherichia coli in extra-intestinal infections. Epidemiol Infect 95:551–575
Piatti G, Mannini A, Balistreri M, Schito AM (2008) Virulence factors in urinary Escherichia coli strains: phylogenetic background and quinolone and fluoroquinolone resistance. J Clin Microbiol 46:480–487. https://doi.org/10.1128/JCM.01488-07
doi: 10.1128/JCM.01488-07
pubmed: 18057134
Rasko DA, Rosovitz MJ, Myers GSA, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893. https://doi.org/10.1128/JB.00619-08
doi: 10.1128/JB.00619-08
pubmed: 18676672
pmcid: 2566221
Salehzadeh A, Zamani H (2018) Characterization of (Uropathogenic) E. coli isolated from urinary tract infections: phylogenetic typing and distribution of virulence-associated traits. Br J Biomed Sci 75:40–42. https://doi.org/10.1080/09674845.2017.1336834
doi: 10.1080/09674845.2017.1336834
pubmed: 28709389
Sawma-Aouad G, Hashwa F, Tokajian S (2009) Antimicrobial resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli in lebanon. J Chemother 21:153–8. https://doi.org/10.1179/joc.2009.21.2.153
doi: 10.1179/joc.2009.21.2.153
pubmed: 19423467
Shah C, Baral R, Bartaula B, Shrestha LB (2019) Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 19:204. https://doi.org/10.1186/s12866-019-1587-3
doi: 10.1186/s12866-019-1587-3
pubmed: 31477018
pmcid: 6720075
Tabasi M, Asadi Karam MR, Habibi M, Yekaninejad MS, Bouzari S (2015) Phenotypic assays to determine virulence factors of uropathogenic Escherichia coli (UPEC) isolates and their correlation with antibiotic resistance pattern. Osong Public Heal Res Perspect 6(2015):261–268. https://doi.org/10.1016/j.phrp.2015.08.002
doi: 10.1016/j.phrp.2015.08.002
Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J (2013) Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J Infec Dis 17(6):e450–e453. https://doi.org/10.1016/j.ijid.2013.01.025
doi: 10.1016/j.ijid.2013.01.025
Tewawong N, Kowaboot S, Pimaingo Y, Watanagul N, Thongmee T, Poovorawan Y (2020) Distribution of phylogenetic groups, adhesin genes, biofilm formation, and antimicrobial resistance of uropathogenic Escherichia coli isolated from hospitalized patients in Thailand. PeerJ 8:e10453. https://doi.org/10.7717/peerj.10453
doi: 10.7717/peerj.10453
pubmed: 33344087
pmcid: 7718785
Trifillis AL, Donnenberg MS, Cui X, Russell RG, Utsalo SJ, Mobley HLT, Warren JW (1994) Binding to and killing of human renal epithelial cells by hemolytic P-fimbriated E. coli. Kidney Int 46:1083–1091. https://doi.org/10.1038/ki.1994.370
doi: 10.1038/ki.1994.370
pubmed: 7861702
Wiles TJ, Kulesus RR, Mulvey MA (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85:11–19. https://doi.org/10.1016/j.yexmp.2008.03.007
doi: 10.1016/j.yexmp.2008.03.007
pubmed: 18482721
pmcid: 2595135
Xia P, Zou Y, Wang Y, Song Y, Liu W, Francis DH, Zhu G (2015) Receptor for the F4 fimbriae of enterotoxigenic Escherichia coli (ETEC). Appl Microbiol Biotechnol 99:4953–4959. https://doi.org/10.1007/s00253-015-6643-9
doi: 10.1007/s00253-015-6643-9
pubmed: 25967654
Yazdanpour Z, Tadjrobehkar O, Shahkhah M (2020) Significant association between genes encoding virulence factors with antibiotic resistance and phylogenetic groups in community acquired uropathogenic Escherichia coli isolates. BMC Microbiol 20(1):1–9. https://doi.org/10.1186/s12866-020-01933-1
doi: 10.1186/s12866-020-01933-1
Yılmaz EŞ, Aslantaş Ö (2020) Phylogenetic group/subgroups distributions, virulence factors, and antimicrobial susceptibility of Escherichia coli strains from urinary tract infections in Hatay. Rev Soc Bras Med Trop 53. https://doi.org/10.1590/0037-8682-0429-2019
Zaki M, Elewa A (2015) Evaluation of uropathogenic virulence genes in Escherichia coli isolated from children with urinary tract infection. Int J Adv Res 3(3):165–173
Clermont O, Dixit OVA, Vangchhia B, Condamine B, Dion S, Bridier-Nahmias A, Denamur E, Gordon D (2019 Aug) Characterization and rapid identification of phylogroup G in Escherichia coli, a lineage with high virulence and antibiotic resistance potential. Environ Microbiol. 21(8):3107–3117. https://doi.org/10.1111/1462-2920.14713
doi: 10.1111/1462-2920.14713
pubmed: 31188527