Molecular characterization of multidrug-resistant Proteus mirabilis isolates from pregnant women with recurrent urinary tract infection in Erbil city, Iraq
Abstract
Background and Objectives: Urinary tract infections (UTIs) are common in pregnancy and can cause maternal and fetal complications. Proteus mirabilis is a significant pathogen in recurrent UTIs due to its virulence factors. This study investigated the virulence genes and antibiotic resistance patterns of P. mirabilis isolates from pregnant women with UTIs in Erbil, Iraq.
Materials and Methods: This cross-sectional study (September 2024–January 2025) included 120 urine specimens from pregnant women (15-44 years) with UTI symptoms. Bacterial identification was performed using culture, biochemical tests, as well as the Vitek 2 system. Virulence genes were detected by PCR, and antimicrobial susceptibility was assessed by standard methods.
Results: Of the 120 samples, 103 (85.8%) showed bacterial growth; 8 (6.7%) were positive for P. mirabilis, while 95 (79.1%) yielded other bacteria. The most affected age group was 25-34 years (52.5%), predominantly in the second trimester (42.5%) and urban residents (60.8%). Antimicrobial resistance was significant to ampicillin, trimethoprim-sulfamethoxazole, amoxicillin/clavulanic acid, and cephalosporins, although susceptibility was observed with several antibiotics. All P. mirabilis isolates harbored the UreC gene, and 75% possessed the MrpA virulence gene.
Conclusion: Multidrug-resistant P. mirabilis with key virulence genes was detected in pregnant women with UTIs. Regular screening and resistance monitoring are essential for effective management.
1. Mancuso G, Midiri A, Gerace E, Marra M, Zummo S, Biondo C. Urinary tract infections: the current scenario and future prospects. Pathogens 2023; 12: 623.
2. 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.
3. Jappi Y, Hadi U. Purple Urine bag Syndrome in urinary tract Infection. J Glob Infect Dis 2023; 15: 84-85.
4. Baimakhanova B, Sadanov A, Trenozhnikova L, Balgimbaeva A, Baimakhanova G, Orasymbet S, et al. Understanding the burden and management of urinary tract infections in women. Diseases 2025; 13: 59.
5. Rodrigues F, Coelho P, Mateus S, Eideh H, Gonçalves T, Caseiro A, et al. Rising trends of urinary infections among pregnant women: insights from a Portuguese hospital (2018–2022). Bacteria 2025; 4: 10.
6. Hussein EF, Ameen JA, Yassen SH. Study the antibiotics activity against Escherichia coli isolated from urine samples of pregnant women with urinary tract infection. Int J Pharm Res 2021; 13: 1368-1372.
7. Balasubramanian S, Wang X, Sahil S, Cheng AL, Sutkin G, Shepherd JP. Risk factors for the development of acute pyelonephritis in women with a positive urine culture. Neurourol Urodyn 2022; 41: 1582-1589.
8. Algburi A, Alazzawi SA, Al-Ezzy AIA, Weeks R, Chistyakov V, Chikindas ML. Potential probiotics Bacillus subtilis KATMIRA1933 and Bacillus amyloliquefaciens B-1895 co-aggregate with clinical isolates of Proteus mirabilis and prevent biofilm formation. Probiotics Antimicrob Proteins 2020; 12: 1471-1483.
9. Zhou Y, Zhou Z, Zheng L, Gong Z, Li Y, Jin Y, et al. Urinary tract infections caused by uropathogenic Escherichia coli: mechanisms of infection and treatment options. Int J Mol Sci 2023; 24: 10537.
10. Al-khalidy RMS, Aburesha RA. Molecular detection of some virulence genes in Proteus mirabilis isolated from urinary tract infections in Iraq. Iraqi J Agric Sci 2023; 54: 709-715.
11. Hassuna NA, Kotb DN, Lami M, Abdelrahim SS. Characterization of antimicrobial resistance among Proteus mirabilis isolates from catheter-associated urinary tract infections and non-catheter-associated urinary tract infections in Egypt. BMC Infect Dis 2025; 25: 767.
12. Ibrahim MA, Faisal RM. Molecular characterization of antibiotic resistance and virulence genes on plasmids of Proteus mirabilis isolated from urine samples of hospitals in Mosul City, Iraq. J Appl Nat Sci 2024; 16: 830-841.
13. Mohammed SO, ElShahaby OA, Elsayed Hafez E, Khalid Mohammed A, ElShahaby O. Characterization and purification of urease enzyme from new Proteus mirabilis strain. J Adv Sci Res 2014; 5: 8-11.
14. Wasfi R, Hamed SM, Amer M, Fahmy LI. Proteus mirabilis biofilm: development and therapeutic strategies. Front Cell Infect Microbiol 2020; 10: 414.
15. Salama LA, Saleh HH, Abdel-Rhman SH, Barwa R, Hassan R. Assessment of typing methods, virulence genes profile and antimicrobial susceptibility for clinical isolates of Proteus mirabilis. Ann Clin Microbiol Antimicrob 2025; 24: 4.
16. Mirzaei A, Habibi M, Bouzari S, Asadi Karam MR. Characterization of antibiotic-susceptibility patterns, virulence factor profiles and clonal relatedness in Proteus mirabilis isolates from patients with urinary tract infection in Iran. Infect Drug Resist 2019; 12: 3967-3979.
17. Phiri RM, Ertuğrul MB, Bozdoğan B, Hoşbul T. Evaluation of virulence genes in Proteus strains isolated from diabetic foot infections and urinary tract infections. J Infect Dev Ctries 2024; 18: 1559-1565.
18. Hussein EI, Al-Batayneh K, Masadeh MM, Dahadhah FW, Al Zoubi MS, Aljabali AA, et al. Assessment of pathogenic potential, virulent genes profile, and antibiotic susceptibility of Proteus mirabilis from urinary tract infection. Int J Microbiol 2020; 2020: 1231807.
19. Ahmed SS, Shariq A, Alsalloom AA, Babikir IH, Alhomoud BN. Uropathogens and their antimicrobial resistance patterns: relationship with urinary tract infections. Int J Health Sci (Qassim) 2019; 13: 48-55.
20. Mansouri F, Sheibani H, Javedani Masroor M, Afsharian M. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae and urinary tract infections in pregnant/postpartum women: a systematic review and meta-analysis. Int J Clin Pract 2019; e13422.
21. Emami A, Javanmardi F, Pirbonyeh N. Antibiotic resistant profile of asymptomatic bacteriuria in pregnant women: a systematic review and meta-analysis. Expert Rev Anti Infect Ther 2020; 18: 807-815.
22. Al-Obaidi SAJ, Al-Hashimy ABJ. Molecular detection of (Urec, Mrpa, Hpma) genes in Proteus mirabilis bacteria isolated from patients with urinary tract infection. Egypt J Hosp Med 2023; 90: 716-720.
23. Getaneh T, Negesse A, Dessie G, Desta MM, Tigabu AA. Prevalence of urinary tract infection and its associated factors among pregnant women in Ethiopia: a systematic review and meta-analysis. Biomed Res Int 2021; 2021: 6551526.
24. Salari N, Khoshbakht Y, Hemmati M, Khodayari Y, Khaleghi AA, Jafari F, et al. Global prevalence of urinary tract infection in pregnant mothers: a systematic review and meta-analysis. Public Health 2023; 224: 58-65.
25. Asmat U, Mumtaz MZ, Malik A. Rising prevalence of multidrug-resistant uropathogenic bacteria from urinary tract infections in pregnant women. J Taibah Univ Med Sci 2020; 16: 102-111.
26. Nahab HM, Akeel Hamed Al-Oebady M, Aqeel Abdul Munem H. Bacteriological study of urinary tract infections among pregnant women in Al-Samawa city of Iraq. Arch Razi Inst 2022; 77: 117-122.
27. Al-Sarray HAK. Prevalence of bacterial urinary tract infection among pregnant women in Wasit Province in Iraq. South East Eur J Public Health 2024; 513-519.
28. Mahdi AG. Isolation and identification of aerobic bacteria causing urinary tract infection in pregnant women in Al-Diwaniya city and its sensitivity to some antibiotics. Iraqi Acad Sci J 2009; 14: 1-12.
29. Taghavi Zahedkalaei A, Kazemi M, Zolfaghari P, Rashidan M, Sohrabi MB. Association between urinary tract infection in the first trimester and risk of preeclampsia: a case–control study. Int J Womens Health 2020; 12: 521-526.
30. Ejerssa AW, Gadisa DA, Orjino TA. Prevalence of bacterial uropathogens and their antimicrobial susceptibility patterns among pregnant women in Eastern Ethiopia: hospital-based cross-sectional study. BMC Womens Health 2021; 21: 291.
31. Shakoor MM. Knowledge of pregnant women toward prevention of urinary tract infection in Kirkuk City. Kufa J Nurs Sci 2023; 13: 19-25.
32. Lazarus JE, Gupta K. Recurrent UTI in women: risk factors and management. Infect Dis Clin North Am 2024; 38: 325-341.
33. Saeed A, Hamid SA, Bayoumi M, Shanan S, Alouffi S, Alharbi SA, et al. Elevated antibiotic resistance of Sudanese urinary tract infection bacteria. EXCLI J 2017; 16: 1073-1080.
34. Rath S, Padhy RN. Surveillance of acute community-acquired urinary tract bacterial infections. J Acute Dis 2015; 4: 186-195.
35. Li X, Chen Y, Gao W, Ye H, Shen Z, Wen Z, et al. A 6-year study of complicated urinary tract infections in southern China: prevalence, antibiotic resistance, clinical and economic outcomes. Ther Clin Risk Manag 2017; 13: 1479-1487.
36. Parmanik A, Das S, Kar B, Bose A, Dwivedi GR, Pandey MM. Current treatment strategies against multidrug-resistant bacteria: a review. Curr Microbiol 2022; 79: 388.
37. Al Obeidi DN, Al Zubaidy ZM, Ammari A. Molecular detection of some virulence factors of uropathogenic Proteus mirabilis using PCR technique. AIP Conf Proc 2023; 2475: 020011.
38. Tabatabaei A, Ahmadi K, Shabestari AN, Khosravi N, Badamchi A. Virulence genes and antimicrobial resistance pattern in Proteus mirabilis strains isolated from patients with urinary infections in tertiary hospitals in Iran. Afr Health Sci 2021; 21: 1677-1684.
39. Danilo de Oliveira W, Lopes Barboza MG, Faustino G, Yamanaka Inagaki WT, Sanches MS, Takayama Kobayashi RK, et al. Virulence, resistance and clonality of Proteus mirabilis isolated from patients with community-acquired urinary tract infection (CA-UTI) in Brazil. Microb Pathog 2021; 152: 104642.
40. Ghaima KK, Hamid HH, Hasan SF. Biofilm formation, antibiotic resistance and detection of mannose-resistant Proteus-like (MR/P) fimbriae genes in Proteus mirabilis isolated from UTI. Int J ChemTech Res 2017; 10: 964-971.
41. Al-Hamdani H, Al-Hashimy A. Molecular detection of UreC, HpmA, RsbA and MrpA genes of Proteus mirabilis urinary tract infection in patient with rheumatoid arthritis. Iraqi J Agric Sci 2020; 51: 245-251.
42. Li Y, Yin M, Fang C, Fu Y, Dai X, Zeng W, et al. Genetic analysis of resistance and virulence characteristics of clinical multidrug-resistant Proteus mirabilis isolates. Front Cell Infect Microbiol 2023; 13: 1229194.
2. 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.
3. Jappi Y, Hadi U. Purple Urine bag Syndrome in urinary tract Infection. J Glob Infect Dis 2023; 15: 84-85.
4. Baimakhanova B, Sadanov A, Trenozhnikova L, Balgimbaeva A, Baimakhanova G, Orasymbet S, et al. Understanding the burden and management of urinary tract infections in women. Diseases 2025; 13: 59.
5. Rodrigues F, Coelho P, Mateus S, Eideh H, Gonçalves T, Caseiro A, et al. Rising trends of urinary infections among pregnant women: insights from a Portuguese hospital (2018–2022). Bacteria 2025; 4: 10.
6. Hussein EF, Ameen JA, Yassen SH. Study the antibiotics activity against Escherichia coli isolated from urine samples of pregnant women with urinary tract infection. Int J Pharm Res 2021; 13: 1368-1372.
7. Balasubramanian S, Wang X, Sahil S, Cheng AL, Sutkin G, Shepherd JP. Risk factors for the development of acute pyelonephritis in women with a positive urine culture. Neurourol Urodyn 2022; 41: 1582-1589.
8. Algburi A, Alazzawi SA, Al-Ezzy AIA, Weeks R, Chistyakov V, Chikindas ML. Potential probiotics Bacillus subtilis KATMIRA1933 and Bacillus amyloliquefaciens B-1895 co-aggregate with clinical isolates of Proteus mirabilis and prevent biofilm formation. Probiotics Antimicrob Proteins 2020; 12: 1471-1483.
9. Zhou Y, Zhou Z, Zheng L, Gong Z, Li Y, Jin Y, et al. Urinary tract infections caused by uropathogenic Escherichia coli: mechanisms of infection and treatment options. Int J Mol Sci 2023; 24: 10537.
10. Al-khalidy RMS, Aburesha RA. Molecular detection of some virulence genes in Proteus mirabilis isolated from urinary tract infections in Iraq. Iraqi J Agric Sci 2023; 54: 709-715.
11. Hassuna NA, Kotb DN, Lami M, Abdelrahim SS. Characterization of antimicrobial resistance among Proteus mirabilis isolates from catheter-associated urinary tract infections and non-catheter-associated urinary tract infections in Egypt. BMC Infect Dis 2025; 25: 767.
12. Ibrahim MA, Faisal RM. Molecular characterization of antibiotic resistance and virulence genes on plasmids of Proteus mirabilis isolated from urine samples of hospitals in Mosul City, Iraq. J Appl Nat Sci 2024; 16: 830-841.
13. Mohammed SO, ElShahaby OA, Elsayed Hafez E, Khalid Mohammed A, ElShahaby O. Characterization and purification of urease enzyme from new Proteus mirabilis strain. J Adv Sci Res 2014; 5: 8-11.
14. Wasfi R, Hamed SM, Amer M, Fahmy LI. Proteus mirabilis biofilm: development and therapeutic strategies. Front Cell Infect Microbiol 2020; 10: 414.
15. Salama LA, Saleh HH, Abdel-Rhman SH, Barwa R, Hassan R. Assessment of typing methods, virulence genes profile and antimicrobial susceptibility for clinical isolates of Proteus mirabilis. Ann Clin Microbiol Antimicrob 2025; 24: 4.
16. Mirzaei A, Habibi M, Bouzari S, Asadi Karam MR. Characterization of antibiotic-susceptibility patterns, virulence factor profiles and clonal relatedness in Proteus mirabilis isolates from patients with urinary tract infection in Iran. Infect Drug Resist 2019; 12: 3967-3979.
17. Phiri RM, Ertuğrul MB, Bozdoğan B, Hoşbul T. Evaluation of virulence genes in Proteus strains isolated from diabetic foot infections and urinary tract infections. J Infect Dev Ctries 2024; 18: 1559-1565.
18. Hussein EI, Al-Batayneh K, Masadeh MM, Dahadhah FW, Al Zoubi MS, Aljabali AA, et al. Assessment of pathogenic potential, virulent genes profile, and antibiotic susceptibility of Proteus mirabilis from urinary tract infection. Int J Microbiol 2020; 2020: 1231807.
19. Ahmed SS, Shariq A, Alsalloom AA, Babikir IH, Alhomoud BN. Uropathogens and their antimicrobial resistance patterns: relationship with urinary tract infections. Int J Health Sci (Qassim) 2019; 13: 48-55.
20. Mansouri F, Sheibani H, Javedani Masroor M, Afsharian M. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae and urinary tract infections in pregnant/postpartum women: a systematic review and meta-analysis. Int J Clin Pract 2019; e13422.
21. Emami A, Javanmardi F, Pirbonyeh N. Antibiotic resistant profile of asymptomatic bacteriuria in pregnant women: a systematic review and meta-analysis. Expert Rev Anti Infect Ther 2020; 18: 807-815.
22. Al-Obaidi SAJ, Al-Hashimy ABJ. Molecular detection of (Urec, Mrpa, Hpma) genes in Proteus mirabilis bacteria isolated from patients with urinary tract infection. Egypt J Hosp Med 2023; 90: 716-720.
23. Getaneh T, Negesse A, Dessie G, Desta MM, Tigabu AA. Prevalence of urinary tract infection and its associated factors among pregnant women in Ethiopia: a systematic review and meta-analysis. Biomed Res Int 2021; 2021: 6551526.
24. Salari N, Khoshbakht Y, Hemmati M, Khodayari Y, Khaleghi AA, Jafari F, et al. Global prevalence of urinary tract infection in pregnant mothers: a systematic review and meta-analysis. Public Health 2023; 224: 58-65.
25. Asmat U, Mumtaz MZ, Malik A. Rising prevalence of multidrug-resistant uropathogenic bacteria from urinary tract infections in pregnant women. J Taibah Univ Med Sci 2020; 16: 102-111.
26. Nahab HM, Akeel Hamed Al-Oebady M, Aqeel Abdul Munem H. Bacteriological study of urinary tract infections among pregnant women in Al-Samawa city of Iraq. Arch Razi Inst 2022; 77: 117-122.
27. Al-Sarray HAK. Prevalence of bacterial urinary tract infection among pregnant women in Wasit Province in Iraq. South East Eur J Public Health 2024; 513-519.
28. Mahdi AG. Isolation and identification of aerobic bacteria causing urinary tract infection in pregnant women in Al-Diwaniya city and its sensitivity to some antibiotics. Iraqi Acad Sci J 2009; 14: 1-12.
29. Taghavi Zahedkalaei A, Kazemi M, Zolfaghari P, Rashidan M, Sohrabi MB. Association between urinary tract infection in the first trimester and risk of preeclampsia: a case–control study. Int J Womens Health 2020; 12: 521-526.
30. Ejerssa AW, Gadisa DA, Orjino TA. Prevalence of bacterial uropathogens and their antimicrobial susceptibility patterns among pregnant women in Eastern Ethiopia: hospital-based cross-sectional study. BMC Womens Health 2021; 21: 291.
31. Shakoor MM. Knowledge of pregnant women toward prevention of urinary tract infection in Kirkuk City. Kufa J Nurs Sci 2023; 13: 19-25.
32. Lazarus JE, Gupta K. Recurrent UTI in women: risk factors and management. Infect Dis Clin North Am 2024; 38: 325-341.
33. Saeed A, Hamid SA, Bayoumi M, Shanan S, Alouffi S, Alharbi SA, et al. Elevated antibiotic resistance of Sudanese urinary tract infection bacteria. EXCLI J 2017; 16: 1073-1080.
34. Rath S, Padhy RN. Surveillance of acute community-acquired urinary tract bacterial infections. J Acute Dis 2015; 4: 186-195.
35. Li X, Chen Y, Gao W, Ye H, Shen Z, Wen Z, et al. A 6-year study of complicated urinary tract infections in southern China: prevalence, antibiotic resistance, clinical and economic outcomes. Ther Clin Risk Manag 2017; 13: 1479-1487.
36. Parmanik A, Das S, Kar B, Bose A, Dwivedi GR, Pandey MM. Current treatment strategies against multidrug-resistant bacteria: a review. Curr Microbiol 2022; 79: 388.
37. Al Obeidi DN, Al Zubaidy ZM, Ammari A. Molecular detection of some virulence factors of uropathogenic Proteus mirabilis using PCR technique. AIP Conf Proc 2023; 2475: 020011.
38. Tabatabaei A, Ahmadi K, Shabestari AN, Khosravi N, Badamchi A. Virulence genes and antimicrobial resistance pattern in Proteus mirabilis strains isolated from patients with urinary infections in tertiary hospitals in Iran. Afr Health Sci 2021; 21: 1677-1684.
39. Danilo de Oliveira W, Lopes Barboza MG, Faustino G, Yamanaka Inagaki WT, Sanches MS, Takayama Kobayashi RK, et al. Virulence, resistance and clonality of Proteus mirabilis isolated from patients with community-acquired urinary tract infection (CA-UTI) in Brazil. Microb Pathog 2021; 152: 104642.
40. Ghaima KK, Hamid HH, Hasan SF. Biofilm formation, antibiotic resistance and detection of mannose-resistant Proteus-like (MR/P) fimbriae genes in Proteus mirabilis isolated from UTI. Int J ChemTech Res 2017; 10: 964-971.
41. Al-Hamdani H, Al-Hashimy A. Molecular detection of UreC, HpmA, RsbA and MrpA genes of Proteus mirabilis urinary tract infection in patient with rheumatoid arthritis. Iraqi J Agric Sci 2020; 51: 245-251.
42. Li Y, Yin M, Fang C, Fu Y, Dai X, Zeng W, et al. Genetic analysis of resistance and virulence characteristics of clinical multidrug-resistant Proteus mirabilis isolates. Front Cell Infect Microbiol 2023; 13: 1229194.
| Files | ||
| Issue | Vol 17 No 5 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i5.19884 | |
| Keywords | ||
| Urinary tract infections Proteus mirabilis Pregnant people Virulence factors Multiple drug resistance | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Mustafa A. Molecular characterization of multidrug-resistant Proteus mirabilis isolates from pregnant women with recurrent urinary tract infection in Erbil city, Iraq. Iran J Microbiol. 2025;17(5):751-760.
