Original Article | J Adv Med Biomed Res. 2023; 31(148): 464-471 Journal of Advances in Medical and Biomedical Research | ISSN:2676-6264 Bacterial Urinary Tract Infections in North West of Iran: A Cross- Sectional Study Erfan Fakheri1 1. 2. 3. 4. , Niloufar Kazemi1 , Narges Moradi1,2 , Bahman Mirzaei3,4* Student Research Committee, Zanjan University of Medical Sciences, Zanjan, Iran Dept. of Life Technologies, University of Turku, Turku, Finland Dept. of Bacteriology, Pasteur Institute of Iran, Tehran, Iran Dept. of Medical Microbiology and Virology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran Article Info ABSTRACT 10.30699/jambs.31.148.464 Received: 2022/08/09; Accepted: 2022/00/20; Published Online: 29 Oct 2023; Use your device to scan and read the article online Corresponding Information: Bahman Mirzaei, Dept. of Bacteriology, Pasteur Institute of Iran, Tehran, Iran E-Mail: dr.bahman.m@gmail.com Background & Objective: Bacteria play a major role in urinary tract infections (UTIs); therefore, it is necessary to be aware of their regional prevalence and the causative pathogens for better prognosis and rapid treatment in clinical settings. This study aims to evaluate the prevalence of bacterial isolates involved in UTI samples and their antibiotics resistance pattern. Materials & Methods: In this cross-sectional study, bacterial infections from 4214 urine samples were analyzed from December 2016 to December 2018. After biochemical tests, disk diffusion susceptibility procedures were performed on all positive clinical cultures, according to CLSI guidelines. The obtained data were sorted and statistically analyzed by SPSS 26. Results: Out of 3582 suspected UTIs samples, 2006 (56%) were females and 1576 (44%) males in the 0-99 years old age range and mainly consisting of middle-aged and elderly patients (62.2%). Escherichia coli (53.43%) and Staphylococcus epidermidis (15.99%) were the most frequent isolates. Among gram negative bacteria, nitrofurantoin and among gram- positive, vancomycin represented the lowest resistance rates at 25.27% and 26.74% respectively. Piperacillin showed the least efficacy with a resistance rate of 76.04%, followed by cefazolin with a 74.94% resistance rate. In gram positive bacteria, vancomycin and gentamicin showed more promise with respective resistance rates of 19.34% and 27.34%. The highest resistance was associated with ampicillin (68.61%) and Trimethoprim/Sulfamethoxazole (66.06%). Conclusion: Alarming resistance rates were observed in ampicillin and piperacillin, which should be taken into account in therapy guidelines in this area. Prevalence of resistant strains can be avoided by developing appropriate healthcare policies and community awareness. Keywords: Antimicrobial Resistance, Bacteria, Hospital-acquired Infection, Urinary Tract Infection Copyright © 2023, This is an original open-access article distributed under the terms of the Creative Commons Attribution-noncommercial 4.0 International License which permits copy and redistribution of the material just in noncommercial usages with proper citation. Introduction Nosocomial infections or healthcare-associated infections (HAIs) are infections that hospitalized patients acquire throughout their period of stay. Symptoms of the disease may appear during the hospitalization or after discharge from the hospital (1). Infections that appear after 48 to 72 hours are usually classified as nosocomial, and if the infection occurs less than 48 hours of hospitalization, it is likely that the patient might have obtained the infection during the administration process and may have been in the common phase of the disease (2). A recent meta-analysis conducted by Mohammadi et al., from 2001 to 2017, reported a 4.6% overall prevalence rate of HIAs in Iranian hospitals (3). A 2014 CDC report including 183 US hospitals and 11,282 hospitalized Volume 31, September & October 2023 patients indicated that 4% of the patients suffered from one or more HAIs (4). This results in a rise in costs, length of recovery, disabilities and even death amongst patients and attaches great importance to development of regionally studied and validated diagnostic and therapeutic guidelines for these infections. Bacteria are microorganisms that are found in various environments, especially in clinical settings. The ability of bacteria to cause hospital outbreaks and epidemics is indicative of the importance of these microorganisms. Bacteria are mainly labeled as opportunistic pathogens and can create various acquired infections in clinical settings including bacteremia, meningitis, surgical wound infections, urinary tract infections (UTIs), hospitalJournal of Advances in Medical and Biomedical Research Erfan Fakheri et al. 465 acquired pneumonia, etc. (5). UTIs are bacterial infections that affect various parts of the urinary tract. Physiologic and anatomic differences have made UTIs more prevalent among women than men; however, the prevalence rate is similar in elderly males and females (6). Infections of the lower urinary tract and the upper urinary tract are referred to as cystitis (bladder infection) and pyelonephritis (kidney infection), respectively (7). Symptoms of the lower urinary tract infections include frequent urination accompanied by pain (dysuria), while symptoms of pyelonephritis include fever, shivering and flank pain in addition to the symptoms of lower urinary tract infections (8). The main cause of both types of infections is uropathogenic Escherichia coli, a gram negative rodshaped bacterium from the Enterobacteriaceae family (9). The increasing antibiotic resistance and the emergence of multidrug-resistant (MDR) and extensively-drug resistant (XDR) E. coli strains have led to a global health crisis. In most of the infections, the hospital environment is the source and reservoir and, in several studies, it has been observed that environmental pollution has been the source of sudden epidemics caused by bacterial infections (1). Bacteria play an important role in UTIs; therefore, it is necessary to be aware of their prevalence and the causative pathogens for better prognosis, rapid treatment and elimination of the infectious agents in clinical settings. This study aims to evaluate the prevalence of bacterial isolates involved in UTI samples and their antibiotics resistance pattern. Materials and Methods Sample Collection and Culture A cross-sectional study was designed to analyze bacterial infections in a total number of 3582 urine samples collected from ambulatory and hospitalized patients in Valie-Asr hospital in Zanjan, Iran, from December 2016 to December 2018. Samples were initially cultured on MacConkey agar and blood agar (Lioflchem, Italy), according to standard bacteriological protocols and incubated at 37°C for 24 hours (10). Identification of Bacterial Isolates Bergeys̓ microbiology book guidelines were applied for isolate identification (10). Gram staining and conventional media and biochemical tests including catalase, oxidase, Sulfide Indole Motility (SIM), Triple Sugar Iron Agar (TSI), Methyl Red (MR)/VogesProskauer (VP), citrate, sensitivity to specific antibiotic disks, Mannitol Salt Agar, urease, Dnase, etc. (Merck, Germany) were used to confirm the growth of the bacteria. Antibiotic Susceptibility Testing Disk diffusion susceptibility tests were performed on all positive clinical cultures, according to Clinical Laboratory Standard Institute (CLSI) guidelines (11) using the disks (BD BBLTM Sensi DiscTM) containing amikacin (AN) (30 μg), ceftazidime (CAZ) (30 μg), cephalexin (30 μg), levofloxacin (LEV) (5 μg), piperacillin-tazobactam (PI Volume 31, September & October 2023 10 μg) ciprofloxacin (CP) (5 μg), imipenem (IMP) (10 μg), meropenem (MEN) (10 μg), gentamycin (GM) (10 μg), ampicillin (10 µg), ceftriaxone (CRO) (30 µg), cefotaxime (CTX) (30 µg), trimethoprim/sulfamethoxazole (SXT) (25 [1.25/23.75] µg), cefazolin (CZ), cefepime (FEP) (30 μg), nitrofurantoin (FM) (300 µg), oxacillin (CX) (30 μg), and vancomycin (30 µg) (only for gram positive bacteria) (11). American Type Culture Collection (ATCC) standard reference strains (Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 29213) were used as controls. Statistical Analysis The obtained data were sorted and statistically analyzed in SPSS 26 (SPSS Inc., Chicago, IL, USA). Pearson’s chisquare test was used for variable comparison in independent groups and P-values less than 0.05 were considered significant. Ethics approval and consent to participate This study complies with ethical principles and the standards for conducting clinical research and is approved by The Ethics Committee of Zanjan University of Medical Sciences (IR.ZUMS.REC.1398.370).In the current study, all ethical guidelines including Ethics and Consent to participate from the parents have been collected. Results From December 2016 to December 2018, a total number of 6299 urinary, respiratory tract, blood, and stool culture tests were performed for the patients who referred to Valie-Asr Hospital Laboratory in Zanjan, Iran, including 3168 (50.3%) males and 3131 (49.7%) females. Urine culture was the most frequently requested culture (n=3582, 56.87%), followed by sputum (n=1058, 16.8%), blood (n=854, 13.4%) and stool (n=182, 2.9%) cultures. In this study, we analyzed microbial cultures of patients with bacterial infections of the urinary tract and the associated antimicrobial resistance patterns. The study population consisted of a total number of 3582 patients with positive urine cultures (85%), including 2006 (56%) females and 1576 (44%) males in the 0-99 age range. The study population mainly consisted of middle-aged and elderly patients (n=2228, 62.2%), followed by young adults (n=1021, 28.5%). Positive urine cultures were the least frequent among adolescents and children (n=333, 9.3%). The average age of the study population was 63.4 years. With 1275 positive bacterial growth results, the emergency ward had the highest positive culture ratio (35.6%), followed by the following wards: internal (17.8%, n=638), neurosurgery (16.9%, n=605), intensive care unit (11.8%, n=423), infectious diseases (10.4%, n=373), cardiology (3.7%, n=133), surgery (1.6%, n=57), coronary care unit (0.9%, n=32) oncology (0.7%, n=25), and ophthalmology (0.6%, n=21). Journal of Advances in Medical and Biomedical Research 466 Bacterial Uropathogens According to urine cultures results, E. coli and Staphylococcus epidermidis were the most frequently isolated gram negative and gram-positive bacteria from the urine samples with isolation rates of 53.43% and 15.99%, respectively. Table 1 reveals information on the prevalence of the isolated bacteria. Table 1. Prevalence of isolated bacteria from the urine samples of a total number of 3582 patients with positive urine cultures. Isolation frequency (N=3582) Gram Negative Gram Positive Escherichia coli 53.43% (n=1914) Serratia marcescens 5.38% (n=193) Pseudomonas aeruginosa 4.52% (n=162) Klebsiella pneumoniae 4.15% (n=149) Acinetobacter baumanni 0.3% (n=11) Citrobacter freundii 0.16% (n=6) Morganella morganii 0.11% (n=4) Proteus mirabilis 0.08% (n=3) Staphylococcus epidermidis 15.99% (n=537) Group D Streptococci 7.7% (n=279) Staphylococcus saprophyticus 6.19% (n=222) Lactobacillus acidophilus 1.2% (n=44) Viridans streptococci 1% (n=36) Staphylococcus aureus 0.6% (n=22) Among gram negative bacteria, nitrofurantoin and vancomycin represented the lowest resistance rates at 25.27% and 26.74% respectively. Piperacillin showed the least efficacy with a resistance rate of 76.04%, followed by cefazolin which had a resistance rate of 74.94%. Antibiotic susceptibility results of the isolated gram-negative bacteria are demonstrated in Table 2. Table 2. Antibiotic susceptibility pattern of the gram-negative bacteria isolated from 2442 urine samples of the clinical origin and the associated resistance rates. Amikacin Gentamycin Imipenem E. coli S. marce scens P. aerug inosa K. pneu monia A. bum annii C. freu ndii M. morg anii P. mirab ilis Total (N) Number (n) 1914 193 162 149 11 6 4 3 2442 Sensitive 1178 19 47 63 2 4 3 2 1318 Intermedia te 353 3 2 24 2 1 1 1 387 Resistant 383 171 113 62 7 1 0 0 737 Sensitive 1187 15 50 49 6 3 0 3 1313 Intermedia te 76 3 3 2 1 1 1 0 87 Resistant 651 175 109 98 4 2 3 0 1042 Sensitive 1417 19 36 83 2 0 4 2 1563 Intermedia te 95 17 2 14 1 2 0 0 131 Resistant 402 157 124 52 8 4 0 1 748 Sensitive 1531 10 130 18 1 1 2 0 1693 Volume 31, September & October 2023 Resistan ce Rate (%) 30.18 42.67 30.63 25.27 Journal of Advances in Medical and Biomedical Research Erfan Fakheri et al. 467 Nitrofurantoi n Trimethopri m/Sulfameth oxazole Ciprofloxacin Cefepime Ceftriaxone Piperacillin Cefazolin Ceftazidime Levofloxacin Ampicillin Cefoxitin E. coli S. marce scens P. aerug inosa K. pneu monia A. bum annii C. freu ndii M. morg anii P. mirab ilis Total (N) Intermedia te 115 2 3 12 0 0 0 0 132 Resistant 268 181 29 119 10 5 2 3 617 Sensitive 670 11 4 31 0 2 2 2 722 Intermedia te 57 2 1 1 0 0 0 0 61 Resistant 1187 180 157 117 11 4 2 1 1659 Sensitive 804 19 36 32 0 4 4 3 902 Intermedia te 4 2 5 1 0 0 0 0 12 Resistant 1106 172 121 116 11 2 0 0 1528 Sensitive 957 10 47 47 5 4 2 1 1073 Intermedia te 57 2 7 11 0 0 2 1 80 Resistant 900 181 108 91 6 2 0 1 1289 Sensitive 756 10 17 38 1 2 2 2 828 Intermedia te 17 2 11 3 3 0 0 0 36 Resistant 1141 181 134 108 7 4 2 1 1578 Sensitive 459 10 37 21 1 0 2 3 533 Intermedia te 38 2 4 3 2 2 1 0 52 Resistant 1417 181 121 125 8 4 1 0 1857 Sensitive 511 4 14 19 0 2 1 2 553 Intermedia te 54 1 0 2 0 1 0 1 59 Resistant 1349 188 148 128 11 3 3 0 1830 Sensitive 924 7 47 50 2 3 0 2 1035 Intermedia te 118 3 11 12 0 1 0 0 145 Resistant 872 183 104 87 9 2 4 1 1262 Sensitive 840 14 39 61 2 2 4 2 964 Intermedi ate 54 3 3 3 2 0 0 1 66 Resistant 1020 176 120 85 7 4 0 0 1412 Sensitive 717 19 41 47 6 2 2 3 837 Intermedi ate 239 7 1 43 1 1 0 0 292 Resistant 958 167 120 59 4 3 2 0 1313 Sensitive 1311 8 21 89 5 5 2 2 1443 Intermedi ate 19 3 5 2 1 1 1 0 32 Resistant 584 182 136 58 5 0 1 1 967 Volume 31, September & October 2023 Resistan ce Rate (%) 67.94 62.57 52.78 64.62 76.04 74.94 51.68 57.82 53.77 39.60 Journal of Advances in Medical and Biomedical Research 468 Bacterial Uropathogens Among gram positive bacteria, vancomycin and gentamicin showed more promise with respective resistance rates of 19.34% and 27.34%. The highest resistance was associated with ampicillin (68.61%) and Trimethoprim/Sulfamethoxazole (66.06%). Antibiotic susceptibility results of the isolated gram-positive bacteria are demonstrated in Table 3. Table 3. Antibiotic susceptibility pattern of the gram-positive bacteria isolated from 1096 urine samples of the clinical origin and the associated resistance rates. Amikacin Gentamicin Imipenem Nitrofurant oin Trimethopr im/ Sulfametho xazole Ciprofloxac in Piperacillin Cefepime Vancomyci n Cefazolin S. epidemidi s Group D Streptococci S. saprohyti cus Viridans streptococc i S. aureus Total (N) Number (n) 537 279 222 36 22 1096 Susceptible 326 93 57 5 8 489 Intermediate 74 10 7 1 0 92 Resistant 137 176 158 30 14 515 Susceptible 397 104 145 30 19 695 Intermediate 23 57 13 2 1 96 Resistant 117 118 64 4 2 305 Susceptible 254 80 109 24 12 479 Intermediate 4 40 8 6 1 59 Resistant 279 159 105 6 9 558 Susceptible 388 224 130 27 18 787 Intermediate 16 11 7 2 1 37 Resistant 133 44 85 7 3 272 Susceptible 191 84 43 20 12 350 Intermediate 12 1 8 1 0 22 Resistant 334 194 171 15 10 724 Susceptible 219 73 65 18 12 387 Intermediate 24 11 14 2 5 56 Resistant 294 195 143 16 5 653 Susceptible 260 78 147 4 5 494 Intermediate 8 16 7 3 3 37 Resistant 269 185 68 29 14 565 Susceptible 281 93 58 5 17 454 Intermediate 25 12 6 0 3 46 Resistant 231 174 158 31 2 596 Susceptible 517 176 119 31 19 862 Intermediate 12 6 3 0 1 22 Resistant 8 97 100 5 2 212 Susceptible 329 42 34 17 18 440 Intermediate 9 8 7 4 2 30 Resistant 199 229 181 15 2 626 Susceptible 134 164 22 12 15 347 Intermediate 11 33 4 6 1 55 Resistance rate (%) 46.99 27.83 50.91 24.82 66.06 59.58 51.55 54.38 19.34 57.12 63.32 Oxacillin Volume 31, September & October 2023 Journal of Advances in Medical and Biomedical Research Erfan Fakheri et al. 469 Ampicillin Levofloxaci n S. epidemidi s Group D Streptococci S. saprohyti cus Viridans streptococc i S. aureus Total (N) Resistant 392 82 196 18 6 694 Susceptible 119 93 86 14 7 319 Intermediate 6 14 3 1 1 25 Resistant 412 172 133 21 14 752 Susceptible 253 159 93 4 9 518 Intermediate 10 2 4 2 1 19 Resistant 274 118 125 30 13 560 Resistance rate (%) 68.61 51.09 Discussion A total number of 3582 ambulatory and hospitalized patients with bacterial UTI were included in our study. The overall prevalence of UTI was significantly high (85%, P<0.001) among the patients with a urine culture request compared to several similar studies, which reported overall UTI prevalence of 12.1% to 45.32% (12-15). Even though this prevalence variation can be due to geographical and environmental factors, diagnostic methods applied in the study and the characteristics of the included patients such as personal hygiene standards and diet (15), high prevalence ratio in our study raises the concern of sufficiency of the quantity of microbiologic tests requested by the physicians in this clinical setting in Zanjan, Iran from 2016 to 2018. Similar to other studies in this timeframe and as expected from the general epidemiology of UTIs (14), the female patients consisted the majority of the population in our study. Furthermore, a significant increase was observed in the prevalence of UTI with age, given that most of the patients were from the middle-aged and the elderly group (P=0.016). This can be explained by higher number of hospital admission, longer duration of stay and previous antibiotic therapy in the elderly. UTI incidence in women over 60 was 1.7 times higher than the overall incidence in females, putting this group at the highest risk. This result is similar to that of a study by Alós, which reported 20% and 11% UTI prevalence rates in women over 65 years and in the overall population, respectively (16). marcescens usually accounts for 1-2% of HAIs; however, its isolation rate was significantly higher in this study (5.38%) (P<0.001) (18). This reveals that even though S. marcescens rarely causes communityacquired infections, its importance should be taken into account in healthcare settings and as a nosocomial infection, which plays a critical role in hospital outbreaks. S. epidermidis and group D streptococci were the most prevalent gram-positive bacteria in the patient population with respective prevalence rates of 15.99% and 7.7%. This result was consistent with previous literature reporting Enterococcus spp., Staphylococcus spp., and Streptococcus agalactiae as dominant grampositive uropathogens. Gram-positive bacteria nevertheless, are more likely to be contaminants in the urine cultures and should be analyzed along with other factors including symptoms and urine analysis results such as WBC count (19, 20). Lactobacilli-containing samples were excluded from antibiotic susceptibility tests since they are a part of vaginal bacterial flora and commonly indicative of contamination while collecting urine specimens (21). Gram-negative bacteria were the most sensitive and resistant to nitrofurantoin and piperacillin with resistance rates of 25.27% and 76.04%, respectively. Gram-positive bacteria were widely resistant to ampicillin (68.61%) and Trimethoprim/Sulfamethoxazole (66.06%). Gram-negative bacteria were significantly more prevalent (68%) than gram positive-bacteria (32%) in this study (P<0.001) and E. coli was the pathogen behind more than half of the infections. This is in accordance with results from several other studies, which reported the dominance of gram-negative bacteria and especially E. coli in their study populations (12). The second most common gramnegative bacteria -S. marcescens- nevertheless, was not reported to be frequently isolated in UTIs in other studies, as normally, E. coli, K. pneumoniae, P. aeruginosa, Enterobacter, Citrobacter, P. mirabilis are the most common bacterial uropathogens (17). S. These results are in line with resistance patterns reported from Iran and worldwide (3, 12, 17, 22, 23). Vancomycin resistance was relatively low in both gram-negative (26.74%) and gram-positive (19.34%) bacteria. However, it is considered as a last-resort antibiotic and should only be included in the antibiotic therapy regimen according to regional guidelines and only when needed. The vancomycin resistance result in our study was higher compared to that of a UTI study conducted by Mihankhah et al., in northern Iran, in the same timeframe (11.7%) (22). Furthermore, in a study by Khoshbakht et al., conducted in Karaj, Iran in 2013, vancomycin resistance was reported 7.7% (24). This rate was reported lower and under 5% in a ten-year Volume 31, September & October 2023 Journal of Advances in Medical and Biomedical Research 470 Bacterial Uropathogens surveillance European study conducted on the prevalence and susceptibility patterns of UTIassociated bacteria, in 2013 (13). The limitations of the study included exclusive application of conventional biochemical microbiological tests for bacterial identification and not determining resistance-associated genes. Erfan Fakheri contributed to Conceptualization. Narges Moradi and Niloufar Kazemi contributed to data collection, writing and data curation. Acknowledgments The authors are grateful for the support of colleagues in Bacteriology and virology Departments at Zanjan University of Medical Sciences. Conclusion The overall prevalence of UTIs was relatively high in this study, which emphasizes the importance of proper quantity and quality of urine cultures and susceptibility tests, as well as development of novel efficient surveillance guidelines for each area. E. coli and S. epidermidis were the most prevalently isolated uropathogens and there was a notable S. marcescens outbreak in the study timeframe. Alarming resistance rates were observed in ampicillin and piperacillin, which should be taken into account in therapy guidelines in this area. Prevalence of resistant strains can be avoided by developing appropriate healthcare policies and community awareness. Further studies should focus on regional and periodical prevalence and susceptibility patterns of the UTIs, globally. Conflict of Interest The authors declare that they have no competing interests. References 1. Sikora A ZF. Nosocomial infections: StatPearls Publishing; 2021. Available from: [https://www.ncbi.nlm.nih.gov/books/NBK55931 2/] 2. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36(5):309-32. [DOI:10.1016/j.ajic.2008.03.002] [PMID] 3. Responsible genes to antibiotic resistance, genetic relationship between the resistant strains, and investigating any correlations with patient characteristics are not determined and these are the limitations of this study. Moreover, identification of isolates were merely performed taking advantage of biochemical aspect. Mohammadi M, Vaisi Raiegan A, Jalali R, Ghobadi A, Salari N, Barati H. 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An epidemiological study on the prevalence and antibiotic resistance patterns of bacteria isolated from urinary tract infections in central Iran. Avicenna J Clin Microbiol Infect. 2017;4(3): 42214. [DOI:10.5812/ajcmi.42214] 24. Khoshbakht R, Salimi A, Shirzad Aski H, Keshavarzi H. Antibiotic susceptibility of bacterial strains isolated from urinary tract infections in Karaj, Iran. Jundishapour J Microbiol. 2013;6(1):86-90. [DOI:10.5812/jjm.4830] How to Cite This Article: Fakheri E, Kazemi N, Moradi N, Mirzaei B. Bacterial Urinary Tract Infections in North West of Iran: A CrossSectional Study. J Adv Med Biomed Res. 2023; 31(138):464-71. Download citation: BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks Send citation to: Mendeley Zotero Volume 31, September & October 2023 RefWorks Journal of Advances in Medical and Biomedical Research