International Journal of Microbiology and Biotechnology

Submit a Manuscript

Publishing with us to make your research visible to the widest possible audience.

Propose a Special Issue

Building a community of authors and readers to discuss the latest research and develop new ideas.

Research Article |

High Prevalence of Virulence Genes and in Vitro Biofilm Production in Clinical Multidrug-Resistant Escherichia coli in Dakar Senegal

Bacterial virulence is a key factor determining the outcome of each bacterial infection, and virulent bacteria are often associated with high-risk infections. Thus, this study aimed to screen for virulence genes and evaluate the in vitro biofilm formation capacity of multidrug-resistant Escherichia coli isolated in Dakar. For the 16 virulence genes identified by standard polymerase chain reaction (PCR), all 78 ExPEC isolates carried at least four virulence genes. The prevalence of virulence genes was as follows: adhesin genes fimH (98.7%), mrkD (98.7%), papC (46.2%), afaC (9%), and sfa/focDE (1.3%); iron acquisition system genes entB (98.7%), fepA (98.7%), ybtS (93.6%), fyuA (91%), iucA (91%), iucB (91%), iutA (34.6), iroB (6.4%), iroN (6.4%), and toxin genes hlyA (10.3%) and cnf (1 & 2) (10.3%). Seventy-five of the 78 isolates (96.2%) carried at least two adhesin genes and two iron capture system genes. Evaluation of the biofilm formation capacity revealed that all (29/29) hospital-acquired isolates were biofilm producers with (6/29; 20.7%) strong biofilm producers, (15/29; 51.7%) moderate biofilm producers and (8/29; 27.6%) weak biofilm producers. Hospital-acquired isolates carrying papC had a greater biofilm formation capacity than those lacking papC (p < 0.001). The deepening of this type of study on bacterial virulence and hospital bacterial biofilms could lead to improvements in infection investigation, prevention, and therapeutic protocols.

Virulence Genes, Virulence Factors, Extraintestinal Pathogenic Escherichia coli, Biofilms, Biofilm-Associated Infections

APA Style

Komla Mawunyo Dossouvi, Bissoume Sambe Ba, Gora Lo, Issa Ndiaye, Awa Ba-Diallo, et al. (2023). High Prevalence of Virulence Genes and in Vitro Biofilm Production in Clinical Multidrug-Resistant Escherichia coli in Dakar Senegal. International Journal of Microbiology and Biotechnology, 8(4), 69-81. https://doi.org/10.11648/j.ijmb.20230804.11

ACS Style

Komla Mawunyo Dossouvi; Bissoume Sambe Ba; Gora Lo; Issa Ndiaye; Awa Ba-Diallo, et al. High Prevalence of Virulence Genes and in Vitro Biofilm Production in Clinical Multidrug-Resistant Escherichia coli in Dakar Senegal. Int. J. Microbiol. Biotechnol. 2023, 8(4), 69-81. doi: 10.11648/j.ijmb.20230804.11

AMA Style

Komla Mawunyo Dossouvi, Bissoume Sambe Ba, Gora Lo, Issa Ndiaye, Awa Ba-Diallo, et al. High Prevalence of Virulence Genes and in Vitro Biofilm Production in Clinical Multidrug-Resistant Escherichia coli in Dakar Senegal. Int J Microbiol Biotechnol. 2023;8(4):69-81. doi: 10.11648/j.ijmb.20230804.11

Copyright © 2023 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1. Troeger C, Blacker B, Khalil IA, Rao PC, Cao J, Zimsen SRM, et al. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis 2018; 18: 1191–210. https://doi.org/10.1016/S1473-3099(18)30310-4.
2. Vos T, Lim SS, Abbafati C, Abbas KM, Abbasi M, Abbasifard M, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. The Lancet 2020; 396: 1204–22. https://doi.org/10.1016/S0140-6736(20)30925-9.
3. Santella B, Serretiello E, De Filippis A, Folliero V, Iervolino D, Dell’Annunziata F, et al. Lower Respiratory Tract Pathogens and Their Antimicrobial Susceptibility Pattern: A 5-Year Study. Antibiotics 2021; 10: 851. https://doi.org/10.3390/antibiotics10070851.
4. Casadevall A, Pirofski L. The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 2003; 1: 17–24. https://doi.org/10.1038/nrmicro732.
5. Cepas V, Soto SM. Relationship between Virulence and Resistance among Gram-Negative Bacteria. Antibiotics 2020; 9: 719. https://doi.org/10.3390/antibiotics9100719.
6. Beceiro A, Tomás M, Bou G. Antimicrobial Resistance and Virulence: a Successful or Deleterious Association in the Bacterial World? Clin Microbiol Rev 2013; 26: 185–230. https://doi.org/10.1128/CMR.00059-12.
7. Denamur E, Clermont O, Bonacorsi S, Gordon D. The population genetics of pathogenic Escherichia coli. Nat Rev Microbiol 2021; 19: 37–54. https://doi.org/10.1038/s41579-020-0416-x.
8. Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 2003; 5: 449–56. https://doi.org/10.1016/S1286-4579(03)00049-2.
9. Johnson JR, Russo TA. Extraintestinal pathogenic Escherichia coli: “The other bad E coli.” J Lab Clin Med 2002; 139: 155–62. https://doi.org/10.1067/mlc.2002.121550.
10. Pitout J. Extraintestinal Pathogenic Escherichia coli: A Combination of Virulence with Antibiotic Resistance. Front Microbiol 2012; 3.
11. Vihta K-D, Stoesser N, Llewelyn MJ, Quan TP, Davies T, Fawcett NJ, et al. Trends over time in Escherichia coli bloodstream infections, urinary tract infections, and antibiotic susceptibilities in Oxfordshire, UK, 1998–2016: a study of electronic health records. Lancet Infect Dis 2018; 18: 1138–49. https://doi.org/10.1016/S1473-3099(18)30353-0.
12. Camara M, Mane MT, Ba-Diallo A, Dieng A, Diop-Ndiaye H, Karam F, et al. Extended-spectrum beta-lactamase- and carbapenemase-producing Enterobacteriaceae clinical isolates in a Senegalese teaching hospital: A cross sectional study. Afr J Microbiol Res 2017; 11: 1600–5. https://doi.org/10.5897/AJMR2017.8716.
13. Ouedraogo A-S, Sanou M, Kissou A, Sanou S, Solaré H, Kaboré F, et al. High prevalence of extended-spectrum ß-lactamase producing enterobacteriaceae among clinical isolates in Burkina Faso. BMC Infect Dis 2016; 16: 326. https://doi.org/10.1186/s12879-016-1655-3.
14. Rezatofighi SE, Mirzarazi M, Salehi M. Virulence genes and phylogenetic groups of uropathogenic Escherichia coli isolates from patients with urinary tract infection and uninfected control subjects: a case-control study. BMC Infect Dis 2021; 21: 361. https://doi.org/10.1186/s12879-021-06036-4.
15. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Distribution of virulence genes and phylogenetics of uropathogenic Escherichia coli among urinary tract infection patients in Addis Ababa, Ethiopia. BMC Infect Dis 2020; 20: 108. https://doi.org/10.1186/s12879-020-4844-z.
16. Alqasim A, Abu Jaffal A, Almutairi N, Arshad M, Alyousef AA. Isolation, phenotypic and genotypic characterization of Escherichia coli from the bloodstream samples in Riyadh, Saudi Arabia. J King Saud Univ - Sci 2020; 32: 1464–9. https://doi.org/10.1016/j.jksus.2019.11.043.
17. Lefort A, Panhard X, Clermont O, Woerther P-L, Branger C, Mentré F, et al. Host Factors and Portal of Entry Outweigh Bacterial Determinants To Predict the Severity of Escherichia coli Bacteremia. J Clin Microbiol 2011; 49: 777–83. https://doi.org/10.1128/JCM.01902-10.
18. Abernethy JK, Johnson AP, Guy R, Hinton N, Sheridan EA, Hope RJ. Thirty day all-cause mortality in patients with Escherichia coli bacteraemia in England. Clin Microbiol Infect 2015; 21: 251. e1-251. e8. https://doi.org/10.1016/j.cmi.2015.01.001.
19. Bleibtreu A. Déterminants de la virulence extra-intestinale de Escherichia coli: de la microbiologie à la clinique. J Anti-Infect 2016; 18: 45–51. https://doi.org/10.1016/j.antinf.2016.01.008.
20. Desvaux M, Dalmasso G, Beyrouthy R, Barnich N, Delmas J, Bonnet R. Pathogenicity Factors of Genomic Islands in Intestinal and Extraintestinal Escherichia coli. Front Microbiol 2020; 11.
21. Dale AP, Woodford N. Extra-intestinal pathogenic Escherichia coli (ExPEC): Disease, carriage and clones. J Infect 2015; 71: 615–26. https://doi.org/10.1016/j.jinf.2015.09.009.
22. Javed S, Mirani ZA, Pirzada ZA. Phylogenetic Group B2 Expressed Significant Biofilm Formation among Drug Resistant Uropathogenic Escherichia coli. Libyan J Med 2021; 16: 1845444. https://doi.org/10.1080/19932820.2020.1845444.
23. Rafaque Z, Abid N, Liaqat N, Afridi P, Siddique S, Masood S, et al.

In-vitro Investigation of Antibiotics Efficacy Against Uropathogenic Escherichia coli Biofilms and Antibiotic Induced Biofilm Formation at Sub-Minimum Inhibitory Concentration of Ciprofloxacin

. Infect Drug Resist 2020; 13: 2801–10. https://doi.org/10.2147/IDR.S258355.
24. Ballén V, Cepas V, Ratia C, Gabasa Y, Soto SM. Clinical Escherichia coli: From Biofilm Formation to New Antibiofilm Strategies. Microorganisms 2022; 10: 1103. https://doi.org/10.3390/microorganisms10061103.
25. Slettengren M, Mohanty S, Kamolvit W, Linden J van der, Brauner A. Making medical devices safer: impact of plastic and silicone oil on microbial biofilm formation. J Hosp Infect 2020; 106: 155–62. https://doi.org/10.1016/j.jhin.2020.07.011.
26. Srinivasan R, Santhakumari S, Poonguzhali P, Geetha M, Dyavaiah M, Xiangmin L. Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections. Front Microbiol 2021; 12.
27. Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, et al. Bacterial biofilm and associated infections. J Chin Med Assoc 2018; 81: 7–11. https://doi.org/10.1016/j.jcma.2017.07.012.
28. Kudinha T, Kong F. Antibiotic Susceptibility Patterns and Biofilm Production by Uropathogenic Escherichia coli from Reproductive Age Women in a Region of NSW. J Infect Dis Epidemiol 2022; 8: 280. https://doi.org/10.23937/2474-3658/1510280.
29. Choudhary P, Singh S, Agarwal V, Choudhary P, Singh S, Agarwal V. Microbial Biofilms. IntechOpen; 2020. https://doi.org/10.5772/intechopen.90790.
30. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010; 35: 322–32. https://doi.org/10.1016/j.ijantimicag.2009.12.011.
31. Landini P, Antoniani D, Burgess JG, Nijland R. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl Microbiol Biotechnol 2010; 86: 813–23. https://doi.org/10.1007/s00253-010-2468-8.
32. Beloin C, Roux A, Ghigo J-M. Escherichia coli biofilms. Curr Top Microbiol Immunol 2008; 322: 249–89.
33. Zhou F, Wang D, Hu J, Zhang Y, Tan BK, Lin S. Control Measurements of Escherichia coli Biofilm: A Review. Foods 2022; 11: 2469. https://doi.org/10.3390/foods11162469.
34. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 2000; 19: 2803–12. https://doi.org/10.1093/emboj/19.12.2803.
35. Langstraat J, Bohse M, Clegg S. Type 3 Fimbrial Shaft (MrkA) of Klebsiella pneumoniae, but Not the Fimbrial Adhesin (MrkD), Facilitates Biofilm Formation. Infect Immun 2001; 69: 5805–12. https://doi.org/10.1128/IAI.69.9.5805-5812.2001.
36. Bien J, Sokolova O, Bozko P. Role of Uropathogenic Escherichia coli Virulence Factors in Development of Urinary Tract Infection and Kidney Damage. Int J Nephrol 2012; 2012: e681473. https://doi.org/10.1155/2012/681473.
37. Antão E-M, Wieler LH, Ewers C. Adhesive threads of extraintestinal pathogenic Escherichia coli. Gut Pathog 2009; 1: 22. https://doi.org/10.1186/1757-4749-1-22.
38. Lasaro MA, Salinger N, Zhang J, Wang Y, Zhong Z, Goulian M, et al. F1C Fimbriae Play an Important Role in Biofilm Formation and Intestinal Colonization by the Escherichia coli Commensal Strain Nissle 1917. Appl Environ Microbiol 2009; 75: 246–51. https://doi.org/10.1128/AEM.01144-08.
39. Servin AL. Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli. Clin Microbiol Rev 2005; 18: 264–92. https://doi.org/10.1128/CMR.18.2.264-292.2005.
40. Feng Y, Mannion A, Madden CM, Swennes AG, Townes C, Byrd C, et al. Cytotoxic Escherichia coli strains encoding colibactin and cytotoxic necrotizing factor (CNF) colonize laboratory macaques. Gut Pathog 2017; 9: 71. https://doi.org/10.1186/s13099-017-0220-y.
41. Guyer DM, Henderson IR, Nataro JP, Mobley HLT. Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol 2000; 38: 53–66. https://doi.org/10.1046/j.1365-2958.2000.02110.x.
42. Dautin N. Serine Protease Autotransporters of Enterobacteriaceae (SPATEs): Biogenesis and Function. Toxins 2010; 2: 1179–206. https://doi.org/10.3390/toxins2061179.
43. Hancock V, Ferrières L, Klemm P 2008. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology 2008; 154: 167–75. https://doi.org/10.1099/mic.0.2007/011981-0.
44. Rouault TA. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2006; 2: 406–14. https://doi.org/10.1038/nchembio807.
45. de Lorenzo V, Bindereif A, Paw BH, Neilands JB. Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12. J Bacteriol 1986; 165: 570–8.
46. Müller SI, Valdebenito M, Hantke K. Salmochelin, the long-overlooked catecholate siderophore of Salmonella. BioMetals 2009; 22: 691–5. https://doi.org/10.1007/s10534-009-9217-4.
47. Peralta DR, Adler C, Corbalán NS, García ECP, Pomares MF, Vincent PA. Enterobactin as Part of the Oxidative Stress Response Repertoire. PLOS ONE 2016; 11: e0157799. https://doi.org/10.1371/journal.pone.0157799.
48. May T, Okabe S. Enterobactin is required for biofilm development in reduced-genome Escherichia coli. Environ Microbiol 2011; 13: 3149–62. https://doi.org/10.1111/j.1462-2920.2011.02607.x.
49. Wang S, Niu C, Shi Z, Xia Y, Yaqoob M, Dai J, et al. Effects of ibeA Deletion on Virulence and Biofilm Formation of Avian Pathogenic Escherichia coli. Infect Immun 2011; 79: 279–87. https://doi.org/10.1128/IAI.00821-10.
50. Nie D, Hu Y, Chen Z, Li M, Hou Z, Luo X, et al. Outer membrane protein A (OmpA) as a potential therapeutic target for Acinetobacter baumannii infection. J Biomed Sci 2020; 27: 26. https://doi.org/10.1186/s12929-020-0617-7.
51. Dossouvi K, Samb-Ba B, Lo G, Cissé A, Diallo A, Ndiaye I, et al. Molecular Characterization of Extended-Spectrum Beta-Lactamase-Producing Extra-Intestinal Pathogenic Escherichia coli Isolated in an University Teaching Hospital Dakar-Senegal. Austin J Microbiol 2022.
52. Stepanović S, Vuković D, Jezek P, Pavlović M, Svabic-Vlahović M. Influence of dynamic conditions on biofilm formation by staphylococci. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol 2001; 20: 502–4. https://doi.org/10.1007/s100960100534.
53. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175–9. https://doi.org/10.1016/s0167-7012(00)00122-6.
54. Ghaffoori Kanaan MH, Al-Shadeedi SMJ, Al-Massody AJ, Ghasemian A. Drug resistance and virulence traits of Acinetobacter baumannii from Turkey and chicken raw meat. Comp Immunol Microbiol Infect Dis 2020; 70: 101451. https://doi.org/10.1016/j.cimid.2020.101451.
55. Abdulhasan GA. The Biological Effect of Rosmarinus officinelis L. Essential Oil on Biofilm Formation and Some Fimbrial Genes (fimH-1 and mrkD) of Klebseilla pneumoniae. Iraqi J Sci 2015.
56. Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J Infect Dis 2013; 17: e450–3. https://doi.org/10.1016/j.ijid.2013.01.025.
57. Messai Y, Atmani S, Alouache S, Fernández Pérez R, Estepa V, Torres C, et al. Virulence characteristics and genetic background of ESBL-producing Klebsiella pneumoniae isolates from wastewater Antibiotic resistance View project VIRULENCE CHARACTERISTICS AND GENETIC BACKGROUND OF ESBL-PRODUCING KLEBSIELLA PNEUMONIAE ISOLATES FROM WASTEWATER. 2019. https://doi.org/10.13140/RG.2.2.18462.89927.
58. Searle LJ, Méric G, Porcelli I, Sheppard SK, Lucchini S. Variation in Siderophore Biosynthetic Gene Distribution and Production across Environmental and Faecal Populations of Escherichia coli. PLOS ONE 2015; 10: e0117906. https://doi.org/10.1371/journal.pone.0117906.
59. Johnson JR, Stell AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 2000; 181: 261–72. https://doi.org/10.1086/315217.
60. Dezfulian H, Batisson I, Fairbrother JM, Lau PCK, Nassar A, Szatmari G, et al. Presence and Characterization of Extraintestinal Pathogenic Escherichia coli Virulence Genes in F165-Positive E. coli Strains Isolated from Diseased Calves and Pigs. J Clin Microbiol 2003; 41: 1375–85. https://doi.org/10.1128/JCM.41.4.1375-1385.2003.
61. Firoozeh F, Saffari M, Neamati F, Zibaei M. Detection of virulence genes in Escherichia coli isolated from patients with cystitis and pyelonephritis. Int J Infect Dis 2014; 29: 219–22. https://doi.org/10.1016/j.ijid.2014.03.1393.
62. Zeng Q, Xiao S, Gu F, He W, Xie Q, Yu F, et al. Antimicrobial Resistance and Molecular Epidemiology of Uropathogenic Escherichia coli Isolated From Female Patients in Shanghai, China. Front Cell Infect Microbiol 2021; 11.
63. Tanabe RHS, Dias RCB, Orsi H, de Lira DRP, Vieira MA, dos Santos LF, et al. Characterization of Uropathogenic Escherichia coli Reveals Hybrid Isolates of Uropathogenic and Diarrheagenic (UPEC/DEC) E. coli. Microorganisms 2022; 10: 645. https://doi.org/10.3390/microorganisms10030645.
64. Ballesteros-Monrreal MG, Arenas-Hernández MM, Enciso-Martínez Y, Peña CFM la, Rocha-Gracia R del C, Lozano-Zaraín P, et al.

Virulence and Resistance Determinants of Uropathogenic Escherichia coli Strains Isolated from Pregnant and Non-Pregnant Women from Two States in Mexico

. Infect Drug Resist 2020; 13: 295–310. https://doi.org/10.2147/IDR.S226215.
65. Zhao R, Shi J, Shen Y, Li Y, Han Q, Zhang X, et al. Phylogenetic Distribution of Virulence Genes Among ESBL-producing Uropathogenic Escherichia coli Isolated from Long-term Hospitalized Patients. J Clin Diagn Res JCDR 2015; 9: DC01-04. https://doi.org/10.7860/JCDR/2015/13234.6157.
66. Johnson JG, Murphy CN, Sippy J, Johnson TJ, Clegg S. Type 3 Fimbriae and Biofilm Formation Are Regulated by the Transcriptional Regulators MrkHI in Klebsiella pneumoniae▿. J Bacteriol 2011; 193: 3453–60. https://doi.org/10.1128/JB.00286-11.
67. Khonsari MS, Behzadi P, Foroohi F. The prevalence of type 3 fimbriae in Uropathogenic Escherichia coli isolated from clinical urine samples. Meta Gene 2021; 28: 100881. https://doi.org/10.1016/j.mgene.2021.100881.
68. Mahmoud AT, Ibrahem RA, Salim MT, Gabr A, Halby HM. Prevalence of some virulence factors and genotyping of hospital-acquired uropathogenic Escherichia coli isolates recovered from cancer patients. J Glob Antimicrob Resist 2020; 23: 211–6. https://doi.org/10.1016/j.jgar.2020.08.003.
69. Hyun M, Lee JY, Kim H ah. Differences of virulence factors, and antimicrobial susceptibility according to phylogenetic group in uropathogenic Escherichia coli strains isolated from Korean patients. Ann Clin Microbiol Antimicrob 2021; 20: 77. https://doi.org/10.1186/s12941-021-00481-4.
70. López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, et al. Identification of Virulence Factors Genes in Escherichia coli Isolates from Women with Urinary Tract Infection in Mexico. BioMed Res Int 2014; 2014: e959206. https://doi.org/10.1155/2014/959206.
71. Usein C, Grigore L, Georgescu R, Băltoiu M, Condei M, Teleman M. Phylogenetic background and extraintestinal virulence genotypes of Escherichia coli vaginal strains isolated from adult women Genotipurile de virulen extraintestinal i încadrarea filogenetica tulpinilor vaginale de Escherichia coli izolate de la femei adulte, 2011.
72. Kumar G, Kumar Y, Kumar G, Tahlan AK. Selection and characterization of siderophores of pathogenic Escherichia coli intestinal and extraintestinal isolates. Open Agric 2021; 6: 456–65. https://doi.org/10.1515/opag-2020-0104.
73. Botta A, Barra NG, Lam NH, Chow S, Pantopoulos K, Schertzer JD, et al. Iron Reshapes the Gut Microbiome and Host Metabolism. J Lipid Atheroscler 2021; 10: 160–83. https://doi.org/10.12997/jla.2021.10.2.160.
74. Kurittu P, Khakipoor B, Jalava J, Karhukorpi J, Heikinheimo A. Whole-Genome Sequencing of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli From Human Infections in Finland Revealed Isolates Belonging to Internationally Successful ST131-C1-M27 Subclade but Distinct From Non-human Sources. Front Microbiol 2022; 12: 789280. https://doi.org/10.3389/fmicb.2021.789280.
75. Nesporova K, Wyrsch ER, Valcek A, Bitar I, Chaw K, Harris P, et al. Escherichia coli Sequence Type 457 Is an Emerging Extended-Spectrum-β-Lactam-Resistant Lineage with Reservoirs in Wildlife and Food-Producing Animals. Antimicrob Agents Chemother 2020; 65: e01118-20. https://doi.org/10.1128/AAC.01118-20.
76. Wang H, Xu Q, Chen K, Chan BKW, Ye L, Yang X, et al. A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli. Microbiol Spectr 2022; 10: e0252821. https://doi.org/10.1128/spectrum.02528-21.
77. Abroshan R, Shaheli M. Evaluation of the Frequency of the Uropathogenic Escherichia coli Genotypes Resistant to Multidrug using the iucA, iucB, iucC, and iucD Siderophore Genes. J Ilam Univ Med Sci 2021; 29: 32–42. https://doi.org/10.52547/sjimu.29.2.32.
78. Divya SP, Hatha AAM. Screening of tropical estuarine water in south-west coast of India reveals emergence of ARGs-harboring hypervirulent Escherichia coli of global significance. Int J Hyg Environ Health 2019; 222: 235–48. https://doi.org/10.1016/j.ijheh.2018.11.002.
79. El-Lababidi RM, Rizk JG. Cefiderocol: A Siderophore Cephalosporin. Ann Pharmacother 2020; 54: 1215–31. https://doi.org/10.1177/1060028020929988.
80. Karakonstantis S, Rousaki M, Kritsotakis EI. Cefiderocol: Systematic Review of Mechanisms of Resistance, Heteroresistance and In Vivo Emergence of Resistance. Antibiotics 2022; 11: 723. https://doi.org/10.3390/antibiotics11060723.
81. Khasheii B, Mahmoodi P, Mohammadzadeh A. Siderophores: Importance in bacterial pathogenesis and applications in medicine and industry. Microbiol Res 2021; 250: 126790. https://doi.org/10.1016/j.micres.2021.126790.
82. Brumbaugh AR, Smith SN, Subashchandrabose S, Himpsl SD, Hazen TH, Rasko DA, et al. Blocking Yersiniabactin Import Attenuates Extraintestinal Pathogenic Escherichia coli in Cystitis and Pyelonephritis and Represents a Novel Target To Prevent Urinary Tract Infection. Infect Immun 2015. https://doi.org/10.1128/IAI.02904-14.
83. Habibi M, Asadi Karam MR, Bouzari S. Evaluation of prevalence, immunogenicity and efficacy of FyuA iron receptor in uropathogenic Escherichia coli isolates as a vaccine target against urinary tract infection. Microb Pathog 2017; 110: 477–83. https://doi.org/10.1016/j.micpath.2017.07.037.
84. Larzábal M, Cataldi AA, Vilte DA, Larzábal M, Cataldi AA, Vilte DA. Human and Veterinary Vaccines against Pathogenic Escherichia coli. IntechOpen; 2019. https://doi.org/10.5772/intechopen.82835.
85. Clark JR, Maresso AM. Comparative Pathogenomics of Escherichia coli: Polyvalent Vaccine Target Identification through Virulome Analysis. Infect Immun 2021; 89: e00115-21. https://doi.org/10.1128/IAI.00115-21.
86. Khairy RM, Mohamed ES, Ghany HMA, Abdelrahim SS. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrhegenic E. coli strains isolated from community acquired infections. PLOS ONE 2019; 14: e0222441. https://doi.org/10.1371/journal.pone.0222441.
87. Yun KW, Kim HY, Park HK, Kim W, Lim IS. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J Microbiol Immunol Infect 2014; 47: 455–61. https://doi.org/10.1016/j.jmii.2013.07.010.
88. Ahmed M. GENOTYPIC DETECTION OF THE VIRULENCE FACTORS OF UROPATHOGENIC ESCHERICHIA COLI (UPEC) STRAINS ISOLATED FROM PREGNANT FEMALES AND THEIR CORRELATION WITH ANTIBIOTIC RESISTANCE PATTERN. Al-Azhar J Pharm Sci 2021; 63: 149–72. https://doi.org/10.21608/ajps.2021.153566.
89. Yazdanpour Z, Tadjrobehkar O, Shahkhah M. Significant association between genes encoding virulence factors with antibiotic resistance and phylogenetic groups in community acquired uropathogenic Escherichia coli isolates. BMC Microbiol 2020; 20: 241. https://doi.org/10.1186/s12866-020-01933-1.
90. Meropol SB, Haupt AA, Debanne SM. Incidence and Outcomes of Infections Caused by Multidrug-Resistant Enterobacteriaceae in Children, 2007–2015. J Pediatr Infect Dis Soc 2018; 7: 36–45. https://doi.org/10.1093/jpids/piw093.
91. Dandachi I, Chaddad A, Hanna J, Matta J, Daoud Z. Understanding the Epidemiology of Multi-Drug Resistant Gram-Negative Bacilli in the Middle East Using a One Health Approach. Front Microbiol 2019; 10.
92. Tewawong N, Kowaboot S, Pimainog Y, Watanagul N, Thongmee T, Poovorawan Y. Distribution of phylogenetic groups, adhesin genes, biofilm formation, and antimicrobial resistance of uropathogenic Escherichia coli isolated from hospitalized patients in Thailand. PeerJ 2020; 8: e10453. https://doi.org/10.7717/peerj.10453.
93. Raya S, Belbase A, Dhakal L, Govinda Prajapati K, Baidya R, kishor Bimali N. In-Vitro Biofilm Formation and Antimicrobial Resistance of Escherichia coli in Diabetic and Nondiabetic Patients. BioMed Res Int 2019; 2019: e1474578. https://doi.org/10.1155/2019/1474578.
94. Katongole P, Nalubega F, Florence NC, Asiimwe B, Andia I. Biofilm formation, antimicrobial susceptibility and virulence genes of Uropathogenic Escherichia coli isolated from clinical isolates in Uganda. BMC Infect Dis 2020; 20: 453. https://doi.org/10.1186/s12879-020-05186-1.
95. Schiebel J, Böhm A, Nitschke J, Burdukiewicz M, Weinreich J, Ali A, et al. Genotypic and Phenotypic Characteristics Associated with Biofilm Formation by Human Clinical Escherichia coli Isolates of Different Pathotypes. Appl Environ Microbiol 2017; 83: e01660-17. https://doi.org/10.1128/AEM.01660-17.
96. Fattahi S, Kafil HS, Nahai MR, Asgharzadeh M, Nori R, Aghazadeh M. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg Infect Control 2015; 10: Doc11. https://doi.org/10.3205/dgkh000254.
97. Zamani H, Salehzadeh A. Biofilm formation in uropathogenic Escherichia coli: association with adhesion factor genes. Turk J Med Sci 2018; 48: 162–7. https://doi.org/10.3906/sag-1707-3.
98. Sun J, Marais JPJ, Khoo C, LaPlante K, Vejborg RM, Givskov M, et al. Cranberry (Vaccinium macrocarpon) oligosaccharides decrease biofilm formation by uropathogenic Escherichia coli. J Funct Foods 2015; 17: 235–42. https://doi.org/10.1016/j.jff.2015.05.016.
99. Kim Y-G, Lee J-H, Gwon G, Kim S-I, Park JG, Lee J. Essential Oils and Eugenols Inhibit Biofilm Formation and the Virulence of Escherichia coli O157:H7. Sci Rep 2016; 6: 36377. https://doi.org/10.1038/srep36377.
100. Vikram A, Jesudhasan PR, Pillai SD, Patil BS. Isolimonic acid interferes with Escherichia coli O157:H7 biofilm and TTSS in QseBC and QseA dependent fashion. BMC Microbiol 2012; 12: 261. https://doi.org/10.1186/1471-2180-12-261.
101. Ghosh S, Lahiri D, Nag M, Dey A, Pandit S, Sarkar T, et al. Phytocompound Mediated Blockage of Quorum Sensing Cascade in ESKAPE Pathogens. Antibiot Basel Switz 2022; 11: 61. https://doi.org/10.3390/antibiotics11010061.
102. Gu Y, Xu Y, Xu J, Yu X, Huang X, Liu G, et al. Identification of novel bacteriophage vB_EcoP-EG1 with lytic activity against planktonic and biofilm forms of uropathogenic Escherichia coli. Appl Microbiol Biotechnol 2019; 103: 315–26. https://doi.org/10.1007/s00253-018-9471-x.
103. Moradpour Z, Yousefi N, Sadeghi D, Ghasemian A. Synergistic bactericidal activity of a naturally isolated phage and ampicillin against urinary tract infecting Escherichia coli O157. Iran J Basic Med Sci 2020; 23: 257–63. https://doi.org/10.22038/IJBMS.2019.37561.8989.
104. Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence 2017; 9: 522–54. https://doi.org/10.1080/21505594.2017.1313372.
105. Fleming D, Rumbaugh KP. Approaches to Dispersing Medical Biofilms. Microorganisms 2017; 5: 15. https://doi.org/10.3390/microorganisms5020015.