Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran
Abstract
Background and Objectives: Escherichia coli is known to be the pathogen commonly isolated from those infected with urinary tract infections (UTIs). The aim of this study was to investigate the presence of E. coli virulence genes and antibiotics’ resistance pattern among clinical isolates in the Northeast of Iran. Relationships between virulence genes and antimicrobial resistances were studied as well.
Materials and Methods: Three hundred isolates of E. coli were isolated from patients with UTIs that referred to Ghaem and Imam Reza hospitals (Mashhad, Iran) during August 2016 to February 2017. A multiplex PCR was employed to amplify the genes encoding pyelonephritis associated pili (pap), S-family adhesions (sfa), type1fimbriae (fimH) and aerobactin (aer). Disk diffusion test was performed to test the susceptibility of isolates to β-lactams, aminoglycosides, cephalosporins, quinolone, fluoroquinolones, carbapenems and trimethoprim-sulfamethoxazole.
Results: The PCR results identified the fimH in 78.4%, aer in 70.5%, sfa in 13.6% and the pap in 8.2% of isolates. The rates of antibiotic resistance of the isolates were as follows: 64.7% resistant to cephalosporins, 34% to trimethoprim-sulfamethoxazole, 31% to fluoroquinolones, 15.3% to aminoglycosides, 13.3% to β-lactams, 7.8% to quinolones and 4.4% to carbapenems. Significant relationships existed between pap and aer, pap and sfa, aer and fluoroquinolones also pap and cephalosporins.
Conclusion: fimH and aer were found in > 50% of isolates suggesting the importance of both genes in UPEC. The majority of isolates had fimH as adhesion factor for colonization. Determining antibiotic resistance patterns in specific geographical areas is necessary for appropriate treatment of urinary tract infection. The high rate of resistance to cephalosporins is most likely due to incorrect drug administration.
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2. Hooton TM. Uncomplicated urinary tract infection. N Engl J Med 2012;366:1028-1037.
3. Nielubowicz GR, Mobley HL. Host–pathogen interactions in urinary tract infection. Nat Rev Urol 2010;7:430-441.
4. Pallett A, Hand K. Complicated urinary tract infections: practical solutions for the treatment of multiresistant Gram-negative bacteria. J Antimicrob Chemother 2010;65 Suppl 3:iii25-33.
5. Levison ME, Kaye D. Treatment of complicated urinary tract infections with an emphasis on drug-resistant gram-negative uropathogens. Curr Infect Dis Rep 2013;15:109-115.
6. Smelov V, Naber K, Johansen TEB. Improved classification of urinary tract infection: future considerations. Eur Urol Suppl 2016;15:71-80.
7. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015;13:269-284.
8. Moue A, Aktaruzzaman SA, Ferdous N, Karim MR, Khalil M, Das AK. Prevalence of urinary tract infection in both outpatient department and in patient department at a medical college setting of Bangladesh. Int J Biosci 2015;7:146-152.
9. Sewify M, Nair S, Warsame S, Murad M, Alhubail A, Behbehani K, et al. Prevalence of urinary tract infection and antimicrobial susceptibility among diabetic patients with controlled and uncontrolled glycemia in Kuwait. J Diabetes Res 2016;2016:6573215.
10. 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;2012:681473.
11. Pobiega M, Wojkowska-Mach J, Chmielarczyk A, Romaniszyn D, Adamski P, Heczko PB, et al. Molecular characterization and drug resistance of Escherichia coli strains isolated from urine from long-term care facility residents in Cracow, Poland. Medical science monitor. Med Sci Monit 2013;19:317-326.
12. Slavchev G, Pisareva E, Markova N. Virulence of uropathogenic Escherichia coli. J Cult Collect 2008-2009;6:3-9.
13. Aldous WK, Pounder JI, Cloud JL, Woods GL. Comparison of six methods of extracting Mycobacterium tuberculosis DNA from processed sputum for testing by quantitative real-time PCR. J Clin Microbiol 2005;43:2471-2473.
14. Bahalo S, Tajbakhsh E, Tajbakhsh S, Momeni M, Tajbakhsh F. Detection of some virulence factors of Escherichia coli isolated from urinary tract infection isolated of children in Shahrekord Iran by multiplex PCR. Middle-East J Scien Res 2013;14:29-32.
15. Santo E, Macedo C, Marin JM. Virulence factors of uropathogenic Escherichia coli from a university hospital in Ribeirao Preto, Sao Paulo, Brazil. Rev Inst Med Trop Sao Paulo 2006;48:185-188.
16. Kudinha T, Kong F, Johnson JR, Andrew SD, Anderson P, Gilbert GL. Multiplex PCR-based reverse line blot assay to simultaneously detect 22 virulence genes in uropathogenic Escherichia coli. Appl Environ Microbiol 2011:78:1198-1202.
17. Akoachere J-FTK, Yvonne S, Akum NH, Seraphine EN. Etiologic profile and antimicrobial susceptibility of community-acquired urinary tract infection in two Cameroonian towns. BMC Res Notes 2012;5:219.
18. Farshad S, Emamghorashi F. The prevalence of virulence genes of E. coli strains isolated from children with urinary tract infection. Saudi J Kidney Dis Transpl 2009;20:613-617.
19. Ghazvini H, Taheri K, Edalati E, Sedighi M, Mirkalantar S. Virulence factors and antimicrobial resistance in uropathogenic Escherichia coli strains isolated from cystitis and pyelonephritis. Turk J Med Sci 2019;49:361-367.
20. Staji H, Rassouli M, Jourablou S. Comparative virulotyping and phylogenomics of Escherichia coli isolates from urine samples of men and women suffering urinary tract infections. Iran J Basic Med Sci 2019;22:211-214.
21. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 2019;19:204.
22. Haghighatpanah M, Mojtahedi A. Characterization of antibiotic resistance and virulence factors of Escherichia coli strains isolated from Iranian inpatients with urinary tract infections. Infect Drug Resist 2019;12:2747-2754.
23. 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;47:455-461.
24. Watts RE, Hancock V, Ong C-LY, Vejborg RM, Mabbett AN, Totsika M, et al. Escherichia coli isolates causing asymptomatic bacteriuria in catheterized and noncatheterized individuals possess similar virulence properties. J Clin Microbiol 2010;48:2449-2458.
25. Raeispour M, Ranjbar R. Antibiotic resistance, virulence factors and genotyping of Uropathogenic Escherichia coli strains. Antimicrob Resist Infect Control 2018;7:118.
26. Usein CR, Damian M, Tatu-Chitoiu D, Capusa C, Fagaras R, Tudorache D, et al. Prevalence of virulence genes in Escherichia coli strains isolated from Romanian adult urinary tract infection cases. J Cell Mol Med 2001;5:303-310.
27. 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: 959206.
28. Mladin C, Usein C-R, Chifiriuc M-C, Palade A, Slavu CL, Negut M, et al. Genetic analysis of virulence and pathogenicity features of uropathogenic Escherichia coli isolated from patients with neurogenic bladder. Rom Biotechnol Lett 2009;14:4906-4911.
29. Jalali HR, Pourbakhsh A, Fallah F, Eslami G. Genotyping of virulence factors of Uropathogenic Escherichia coli by PCR. NBM 2015;3:177-181.
30. Hojati Z, Zamanzad B, Hashemzadeh M, Molaie R, Gholipour A. The FimH gene in uropathogenic Escherichia coli strains isolated from patients with urinary tract infection. Jundishapur J Microbiol 2015; 8(2): e17520.
31. 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(6):e450-453.
32. Hassan R, El-Naggar W, El-Sawy E, El-Mahdy A. Characterization of some virulence factors associated with Enterbacteriaceae isolated from urinary tract infections in Mansoura Hospitals. Egypt J Med Microbiol 2011;20:9-17.
33. Sauer MM, Jakob RP, Eras J, Baday S, Eriş D, Navarra G, et al. Catch-bond mechanism of the bacterial adhesin FimH. Nat Commun 2016;7:10738.
34. 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;29:219-222.
35. El-Mosallamy WA, Desouky SM, El-Azm A, Abeer A, Abd El Hamid HS. Detection of some virulence factors and pyelonephritis-associated pilus (pap) encoding operon gene in Uropathogenic Escherichia coli. Egypt J Med Microbiol 2015;24:3;37-43.
36. Fathollahi S, Yousefi_Mashouf R, Goodarzi MT, Hajilooei M, Hemati S, Mostafaei A, et al. Typing of the uropathogenic E. coli strains using. Arch Clin Infect 2009;4:77-81.
37. Derakhshan S, Pourzare M, Roshani D. Distribution of virulence factors according to antibiotic susceptibility among Escherichia coli isolated from urinary tract infection. Indian J Nephrol 2018;28:191-197.
38. Pourzare M, Derakhshan S, Roshani D. Distribution of uropathogenic virulence genes in Escherichia coli isolated from children with urinary tract infection in Sanandaj, Iran. Arch Pediatr Infect Dis 2017;5(3):e41995.
39. Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol 2015; 8(2):e17514.
40. Karimian A, Momtaz H, Madani M. Detection of uropathogenic Escherichia coli virulence factors in patients with urinary tract infections in Iran. Afr J Microbiol Res 2012;39:6811-6816.
41. Hozzari A, Behzadi P, Khiabani PK, Sholeh M, Sabokroo N. Clinical cases, drug resistance, and virulence genes profiling in uropathogenic Escherichia coli. J Appl Genetics 2020; 61:265-273.
42. Sabir S, Anjum AA, Ijaz T, Ali MA. Isolation and antibiotic susceptibility of E. coli from urinary tract infections in a tertiary care hospital. Pak J Med Sci 2014;30:389-392.
43. Taheri M, Saleh M, Nemati AH, Ariana M, Shojaei E, Mardani M, et al. Antibiotic resistance pattern and phylogenetic groups of the Uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. JoMMID 2016;4:76-82.
44. Sharma S, Kaur N, Malhotra S, Madan P, Ahmad W, Hans C. Serotyping and antimicrobial susceptibility pattern of Escherichia coli isolates from urinary tract infections in pediatric population in a tertiary care hospital. J Pathog 2016;2016:2548517.
2. Hooton TM. Uncomplicated urinary tract infection. N Engl J Med 2012;366:1028-1037.
3. Nielubowicz GR, Mobley HL. Host–pathogen interactions in urinary tract infection. Nat Rev Urol 2010;7:430-441.
4. Pallett A, Hand K. Complicated urinary tract infections: practical solutions for the treatment of multiresistant Gram-negative bacteria. J Antimicrob Chemother 2010;65 Suppl 3:iii25-33.
5. Levison ME, Kaye D. Treatment of complicated urinary tract infections with an emphasis on drug-resistant gram-negative uropathogens. Curr Infect Dis Rep 2013;15:109-115.
6. Smelov V, Naber K, Johansen TEB. Improved classification of urinary tract infection: future considerations. Eur Urol Suppl 2016;15:71-80.
7. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015;13:269-284.
8. Moue A, Aktaruzzaman SA, Ferdous N, Karim MR, Khalil M, Das AK. Prevalence of urinary tract infection in both outpatient department and in patient department at a medical college setting of Bangladesh. Int J Biosci 2015;7:146-152.
9. Sewify M, Nair S, Warsame S, Murad M, Alhubail A, Behbehani K, et al. Prevalence of urinary tract infection and antimicrobial susceptibility among diabetic patients with controlled and uncontrolled glycemia in Kuwait. J Diabetes Res 2016;2016:6573215.
10. 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;2012:681473.
11. Pobiega M, Wojkowska-Mach J, Chmielarczyk A, Romaniszyn D, Adamski P, Heczko PB, et al. Molecular characterization and drug resistance of Escherichia coli strains isolated from urine from long-term care facility residents in Cracow, Poland. Medical science monitor. Med Sci Monit 2013;19:317-326.
12. Slavchev G, Pisareva E, Markova N. Virulence of uropathogenic Escherichia coli. J Cult Collect 2008-2009;6:3-9.
13. Aldous WK, Pounder JI, Cloud JL, Woods GL. Comparison of six methods of extracting Mycobacterium tuberculosis DNA from processed sputum for testing by quantitative real-time PCR. J Clin Microbiol 2005;43:2471-2473.
14. Bahalo S, Tajbakhsh E, Tajbakhsh S, Momeni M, Tajbakhsh F. Detection of some virulence factors of Escherichia coli isolated from urinary tract infection isolated of children in Shahrekord Iran by multiplex PCR. Middle-East J Scien Res 2013;14:29-32.
15. Santo E, Macedo C, Marin JM. Virulence factors of uropathogenic Escherichia coli from a university hospital in Ribeirao Preto, Sao Paulo, Brazil. Rev Inst Med Trop Sao Paulo 2006;48:185-188.
16. Kudinha T, Kong F, Johnson JR, Andrew SD, Anderson P, Gilbert GL. Multiplex PCR-based reverse line blot assay to simultaneously detect 22 virulence genes in uropathogenic Escherichia coli. Appl Environ Microbiol 2011:78:1198-1202.
17. Akoachere J-FTK, Yvonne S, Akum NH, Seraphine EN. Etiologic profile and antimicrobial susceptibility of community-acquired urinary tract infection in two Cameroonian towns. BMC Res Notes 2012;5:219.
18. Farshad S, Emamghorashi F. The prevalence of virulence genes of E. coli strains isolated from children with urinary tract infection. Saudi J Kidney Dis Transpl 2009;20:613-617.
19. Ghazvini H, Taheri K, Edalati E, Sedighi M, Mirkalantar S. Virulence factors and antimicrobial resistance in uropathogenic Escherichia coli strains isolated from cystitis and pyelonephritis. Turk J Med Sci 2019;49:361-367.
20. Staji H, Rassouli M, Jourablou S. Comparative virulotyping and phylogenomics of Escherichia coli isolates from urine samples of men and women suffering urinary tract infections. Iran J Basic Med Sci 2019;22:211-214.
21. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 2019;19:204.
22. Haghighatpanah M, Mojtahedi A. Characterization of antibiotic resistance and virulence factors of Escherichia coli strains isolated from Iranian inpatients with urinary tract infections. Infect Drug Resist 2019;12:2747-2754.
23. 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;47:455-461.
24. Watts RE, Hancock V, Ong C-LY, Vejborg RM, Mabbett AN, Totsika M, et al. Escherichia coli isolates causing asymptomatic bacteriuria in catheterized and noncatheterized individuals possess similar virulence properties. J Clin Microbiol 2010;48:2449-2458.
25. Raeispour M, Ranjbar R. Antibiotic resistance, virulence factors and genotyping of Uropathogenic Escherichia coli strains. Antimicrob Resist Infect Control 2018;7:118.
26. Usein CR, Damian M, Tatu-Chitoiu D, Capusa C, Fagaras R, Tudorache D, et al. Prevalence of virulence genes in Escherichia coli strains isolated from Romanian adult urinary tract infection cases. J Cell Mol Med 2001;5:303-310.
27. 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: 959206.
28. Mladin C, Usein C-R, Chifiriuc M-C, Palade A, Slavu CL, Negut M, et al. Genetic analysis of virulence and pathogenicity features of uropathogenic Escherichia coli isolated from patients with neurogenic bladder. Rom Biotechnol Lett 2009;14:4906-4911.
29. Jalali HR, Pourbakhsh A, Fallah F, Eslami G. Genotyping of virulence factors of Uropathogenic Escherichia coli by PCR. NBM 2015;3:177-181.
30. Hojati Z, Zamanzad B, Hashemzadeh M, Molaie R, Gholipour A. The FimH gene in uropathogenic Escherichia coli strains isolated from patients with urinary tract infection. Jundishapur J Microbiol 2015; 8(2): e17520.
31. 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(6):e450-453.
32. Hassan R, El-Naggar W, El-Sawy E, El-Mahdy A. Characterization of some virulence factors associated with Enterbacteriaceae isolated from urinary tract infections in Mansoura Hospitals. Egypt J Med Microbiol 2011;20:9-17.
33. Sauer MM, Jakob RP, Eras J, Baday S, Eriş D, Navarra G, et al. Catch-bond mechanism of the bacterial adhesin FimH. Nat Commun 2016;7:10738.
34. 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;29:219-222.
35. El-Mosallamy WA, Desouky SM, El-Azm A, Abeer A, Abd El Hamid HS. Detection of some virulence factors and pyelonephritis-associated pilus (pap) encoding operon gene in Uropathogenic Escherichia coli. Egypt J Med Microbiol 2015;24:3;37-43.
36. Fathollahi S, Yousefi_Mashouf R, Goodarzi MT, Hajilooei M, Hemati S, Mostafaei A, et al. Typing of the uropathogenic E. coli strains using. Arch Clin Infect 2009;4:77-81.
37. Derakhshan S, Pourzare M, Roshani D. Distribution of virulence factors according to antibiotic susceptibility among Escherichia coli isolated from urinary tract infection. Indian J Nephrol 2018;28:191-197.
38. Pourzare M, Derakhshan S, Roshani D. Distribution of uropathogenic virulence genes in Escherichia coli isolated from children with urinary tract infection in Sanandaj, Iran. Arch Pediatr Infect Dis 2017;5(3):e41995.
39. Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol 2015; 8(2):e17514.
40. Karimian A, Momtaz H, Madani M. Detection of uropathogenic Escherichia coli virulence factors in patients with urinary tract infections in Iran. Afr J Microbiol Res 2012;39:6811-6816.
41. Hozzari A, Behzadi P, Khiabani PK, Sholeh M, Sabokroo N. Clinical cases, drug resistance, and virulence genes profiling in uropathogenic Escherichia coli. J Appl Genetics 2020; 61:265-273.
42. Sabir S, Anjum AA, Ijaz T, Ali MA. Isolation and antibiotic susceptibility of E. coli from urinary tract infections in a tertiary care hospital. Pak J Med Sci 2014;30:389-392.
43. Taheri M, Saleh M, Nemati AH, Ariana M, Shojaei E, Mardani M, et al. Antibiotic resistance pattern and phylogenetic groups of the Uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. JoMMID 2016;4:76-82.
44. Sharma S, Kaur N, Malhotra S, Madan P, Ahmad W, Hans C. Serotyping and antimicrobial susceptibility pattern of Escherichia coli isolates from urinary tract infections in pediatric population in a tertiary care hospital. J Pathog 2016;2016:2548517.
| Files | ||
| Issue | Vol 12 No 3 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i3.3240 | |
| Keywords | ||
| Urinary tract infections; Escherichia coli; Virulence factor; Multiplex polymerase chain reaction; Antibacterial drugs resistance | ||
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How to Cite
1.
Ghavidel M, Gholamhosseini-Moghadam T, Nourian K, Ghazvini K. Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran. Iran J Microbiol. 2020;12(3):223-230.
