Epidemiological insights into seasonal, sex‑specific and age‑related distribution of bacterial pathogens in urinary tract infections
- Authors:
- Published online on: February 14, 2024 https://doi.org/10.3892/etm.2024.12428
- Article Number: 140
Abstract
Introduction
Urinary tract infections (UTIs) are an extensive and pervasive health concern, ranking among the most common and recurring bacterial infections, impacting a vast number of individuals worldwide each passing year (1-4). From 1990 to 2019, the total cases of UTIs surged by 60.40%, rising from 252.25 million to 404.61 million (2). These infections affect people of all ages, backgrounds, and geographical locations, representing a substantial burden on healthcare systems and impacting the overall well-being of affected populations (5,6).
Given the wide-ranging prevalence of UTIs, a comprehensive exploration of their epidemiology and underlying factors becomes of paramount necessity (2,7). Investigating the seasonal distribution of UTIs can shed light on potential environmental and climatic influences, helping identify periods of heightened risk and enabling more proactive public health interventions (8,9). Furthermore, understanding the sex-specific patterns of UTI occurrence can provide valuable insights into the complex interplay between anatomical differences, hormonal factors and behavioral aspects that may contribute to susceptibility (10,11).
Age-related distribution of bacterial pathogens in UTIs is another crucial area of investigation (12). Age has been associated with the incidence of UTIs and with treatment failure of UTIs in multiple observational studies, sometimes yielding conflicting results (13-15). Therefore, recognizing how UTI incidence varies across different age groups can aid in the development of targeted prevention strategies and tailor-made treatment approaches, considering the unique physiological and immunological characteristics of specific populations (16,17).
A heightened understanding of the factors contributing to the development and spread of UTIs can pave the way for the implementation of effective public health measures, including educational campaigns to raise awareness about preventive practices and hygiene habits (18). Community-wide efforts can thus foster a culture of proactive health management, ultimately reducing the incidence of UTIs and improving the overall quality of life for individuals worldwide (2,19).
However, the distribution of bacterial pathogens in UTIs is not well understood, especially regarding seasonal, sex-specific and age-related patterns, creating a crucial knowledge gap. The present study aimed to address this gap by investigating the prevalence and distribution of UTI bacterial pathogens in hospitalized cases, and exploring their complex interaction with various demographic characteristics. The valuable insights gained from this research are expected to result in more effective diagnosis, treatment and prevention strategies. With this knowledge, the impact of UTIs can be proactively mitigated, ultimately promoting better health outcomes and well-being for individuals.
Patients and methods
Study design
This study employed a retrospective observational design to investigate the seasonal, sex-specific and age-related distribution of bacterial pathogens in UTIs. A total of 926 consecutive patients diagnosed with UTIs in Fuding Hospital (Fujian University of Traditional Chinese Medicine, Fuding, China) were enrolled. The patients included 343 men and 583 women diagnosed with UTIs. The data collection period spanned from July 1, 2022, to June 30, 2023. Data from electronic medical records and laboratory reports were collected and analyzed to identify patterns of bacterial prevalence.
Inclusion and exclusion criteria
Inclusion criteria were as follows: Participants with three urine samples exhibiting >105 colony-forming units (CFU)/ml were included. Clean catch midstream urine samples were obtained following proper instructions. Exclusion criteria included participants with inflammatory conditions unrelated to UTIs, those with cancer and pregnant patients.
Data collection and outcome measures
Data were obtained from 926 patients diagnosed with UTIs in Fuding Hospital between July 1, 2022, and June 30, 2023. Demographic information, including age and sex, was extracted from electronic health records. Additionally, information on the date of UTI diagnosis was recorded to categorize cases according to seasonal variations.
Urine samples were obtained through either bladder catheterization or the midstream clean catch method. The urine specimens for routine urinalysis were tested using a Fully Automated Urine Chemistry Analyzer UC-3500 and a Partical Analyzer UF-5000 (Sysmex Corporation). Pyuria was defined as the presence of >5 white blood cells per high-power field in the urine sediment, and significant bacteriuria was identified as the growth of a single pathogenic microorganism >100,000 CFU per ml of urine (20). Patients exhibiting pyuria in the urine analysis underwent a urine culture to confirm the presence of a UTI and detect the causative organism. Cultures were performed using cysteine, lactose, and electrolyte-deficient agar. The culture was considered positive when it detected the presence of at ≥50,000 CFUs per ml of a single urinary pathogen (21). Bacterial isolates derived from urine cultures underwent identification processes that integrated conventional microbiological techniques with the Microbial Analyzing System of VITEKR 2 COMPACT (BioMérieux, Inc.) (22). This comprehensive approach involved methodologies such as Gram staining and biochemical tests. For Gram staining, a standard procedure was followed at room temperature. Bacterial smears were first fixed to a slide by passing through a flame. The slide was then stained with crystal violet for 1 min, followed by the application of iodine solution for 1 min. After a brief rinse with water, the slide was decolorized with alcohol for 20 sec and then counterstained with safranin for 30 sec. The slides were observed under a light microscope at x1,000 magnification. The classification of bacterial species into either Gram-positive or Gram-negative groups was established based on their unique responses to Gram staining.
The reference strains (Escherichia coli, ATCC 25922; Staphylococcus aureus, ATCC 25923; Pseudomonas aeruginosa, ATCC 27853; and Enterococcus faecalis, ATCC 29212) were utilized as positive controls and were all obtained from Fujian Provincial Inspection Center of China.
Classification based on season, sex and age
To examine the seasonal distribution of bacterial pathogens, UTI cases were categorized into four seasons: Spring, summer, autumn and winter, based on the date of UTI diagnosis and corresponding calendar months.
Patients were classified into two sex groups: Male and female, based on their recorded sex in the electronic health records.
Age-related distribution of bacterial pathogens was explored by categorizing patients into four groups: Age group 1, 0-49 years; age group 2, 50-69 years; age group 3, 70-79 years; and age group 4, ≥80 years.
Ethics
The present study was conducted in accordance with ethical guidelines and received approval from the Medical Ethics Committee of Fuding Hospital, Fujian University of Traditional Chinese Medicine (approval no. Fuding Hospital 2022325). The requirement for written informed consent was waived by the Medical Ethics Committee of Fuding Hospital, Fujian University of Traditional Chinese Medicine, due to the retrospective nature of the study.
Statistical analysis
Statistical analysis was conducted using SPSS version 22.0 software (IBM Corp.) and GraphPad Prism 8.0 (Dotmatics). Count data were expressed as n (%). Data normality was assessed using the Kolmogorov-Smirnov test. For non-normally distributed measurements, medians and interquartile ranges were reported. Non-parametric tests were analyzed with the Kruskal-Wallis H test for multiple groups. χ2 tests or Fisher's exact tests, as appropriate, were used to determine the significance of differences in bacterial prevalence across different seasons, sexes and age groups. P<0.05 was considered to indicate a statistically significant difference.
To address the issue of multiple comparisons within the four groups, the Bonferroni correction was applied as a post-hoc analysis after initial tests (Kruskal-Wallis H test and χ2 tests) to indicate significant differences. With six possible pairwise comparisons (4 groups choose 2), the adjusted significance level (ɑadjusted) was calculated as ɑ/6 ≈ 0.0083(23).
Results
The age distribution of the subjects in the four seasonal groups was tested using the Kolmogorov-Smirnov test, yielding results of Z=0.118-0.140, all P<0.001. These results indicated a non-normal distribution of age data, prompting the use of the non-parametric Kruskal-Wallis H test for statistical analysis. Additionally, a χ2 test was performed to compare sex distribution among the four groups. The results of both the sex and age tests are documented in Table I. The statistical analysis revealed that there was no statistically significant difference in age or sex distribution among the four seasonal groups (P>0.05).
A total of 926 bacterial strains were isolated from the studied patients, with 280 (30.2%) belonging to Gram-positive bacteria and 646 (69.8%) to Gram-negative bacteria. Among these, the top nine pathogenic bacteria were identified as follows: E. coli (50.0%), Enterococcus faecium (15.6%), E. faecalis (9.6%), Klebsiella pneumoniae (6.8%), P. aeruginosa (3.5%), A. baumannii (2.7%), Streptococcus agalactiae (2.5%), S. aureus (2.1%) and Proteus mirabilis (1.2%). The remaining bacterial species accounted for 6.2% of the total isolates (Fig. 1).
Further analysis of specific bacterial species revealed associations with the different seasons: E. faecium demonstrated a substantial prevalence during the spring season, with 22.0% of isolates (P=0.005); A. baumannii displayed a notable association with the autumn season, accounting for 5.9% of isolates (P=0.001) (Table II).
 | Table IIAssociation between season and distribution of bacteria (n=926) in urinary tract infections. |
A total of 926 hospitalized subjects were enrolled in the study, including 343 (37.0%) men and 583 (63.0%) women. Gram-positive bacteria were found to be more prevalent in men compared with women (35.9 vs. 26.9%; P=0.004). Particularly, E. faecalis and S. aureus showed significant sex differences, being more common in men (12.5%, P=0.021; and 4.4%, P<0.001, respectively). Furthermore, among Gram-negative bacteria, P. aeruginosa and A. baumannii demonstrated notable sex disparities, with a higher prevalence in men compared with women (7.4%, P=0.001; and 5.0%, P=0.001, respectively). Conversely, E. coli exhibited a higher prevalence in women compared with men (60.4%, P<0.001) (Table III).
The data in Table IV revealed associations between age groups and the prevalence of bacterial pathogens in UTIs. Gram-positive bacteria demonstrated a significant increase in prevalence in the older age groups (age groups 3 and 4) (≥70 years old) (P=0.005), indicating that these bacterial species are more commonly found in elderly patients. Additionally, E. faecium exhibited notable age-related associations (P<0.001), being more prevalent in age groups 3 and 4 (≥70 years old) (18.4 and 23.8%) compared with that in the other age groups.
Among the Gram-negative bacteria, E. coli showed a significant age association (P=0.005). Notably, a higher prevalence was observed in younger age groups, with the highest proportion in the 50-69 years age group (57.3%) and ≤50 years age group (49.2%) (Table IV).
The findings in Table IV suggested that the prevalence of certain bacterial pathogens in UTIs was influenced by the age of the patients. Gram-positive bacteria, E. faecium tended to be more prevalent in older patients, while E. coli was more common in younger patients.
Discussion
The present study sheds light on the distribution of bacterial pathogens in UTIs concerning seasonality, sex, and age factors. The predominant pathogenic bacteria identified were E. coli (50.0%), E. faecium (15.6%), E. faecalis (9.6%), K. pneumoniae (6.8%), P. aeruginosa (3.5%), A. baumannii (2.7%), S. agalactiae (2.5%), S. aureus (2.1%) and P. mirabilis (1.2%). These findings align with those of previous studies (24-26). Another similar study by Faine et al (27) showed that among the patients with positive urine cultures, 84.7% had cultures that grew Enterobacterales, with E. coli (63.2%) being the most common pathogen isolated. Pathogenic E. coli was regarded as the most common pathogen of UTIs (27-30). The present analysis of seasonal distribution revealed a significant association between specific bacterial species and particular seasons. Notably, E. faecium showed higher prevalence during the spring and A. baumannii during the autumn. These findings aligned with a previous study by Alrashid et al (31), which also demonstrated a seasonal pattern, with the highest number of confirmed UTIs in January and the lowest in April. These results emphasized the seasonal variations in UTIs and suggested that the prevalence of bacterial pathogens was influenced by seasonal factors (9). This complexity adds to our understanding of UTIs and highlights the need to consider seasonal variations while devising diagnostic and preventive strategies, as corroborated by the previous study by Simmering et al (8).
The study enrolled a total of 926 hospitalized subjects, with 343 (37.0%) men and 583 (63.0%) women, indicating a higher incidence of UTIs in women, which is consistent with previous studies (5,32,33). UTIs were much more common in women than in men due to certain anatomical and physiological characteristics, such as a shorter urethra, the proximity of the urethral opening to the anus, changes during menopause, pregnancy and other factors, with this difference increasing with age (34,35). The analysis of sex distribution revealed noteworthy differences in the prevalence of bacterial pathogens between male and female groups. Men with UTIs exhibited a greater susceptibility to Gram-positive bacterial infections compared with their female counterparts (35.9 vs. 26.9%; P=0.004). E. faecalis, S. aureus, P. aeruginosa and A. baumannii showed a significant sex difference, being more common in men. Silva et al (36) observed a higher prevalence of UTIs caused by E. faecalis and P. aeruginosa in men compared with women (8.8% for E. faecalis and 8.1% for P. aeruginosa in men, compared with 1.8 and 1.6% in females, respectively). A previous study conducted by Magliano et al (37) demonstrated that P. aeruginosa was found more frequently in men, whereas the prevalence of E. faecalis aligned with the findings of the current study. In the present study, the occurrence of E. faecalis in men and women was 12.5 vs. 7.9% (P<0.05), compared with 9.5 vs. 5.4% (P<0.05) as reported by Magliano et al (37). E. coli. demonstrated notable sex disparities, with a higher prevalence in women compared with men (P<0.001). Amna et al (38) determined that non-E. coli bacteria were more prone to infect men, citing the increased complexity of UTIs in men, often attributed to the frequent use of catheters (39,40). Specifically, Enterococcus and Pseudomonas have been linked to infections associated with urinary tract catheters (41,42). These findings shed light on the intricate interplay between biological, anatomical and behavioral factors in UTI prevalence.
The higher occurrence of Gram-positive bacteria in men suggests the possibility of sex-related disparities in immunity or physiological factors that may render men more susceptible to UTIs (11,43). The finding of the present study, showing a rise in S. aureus among men, aligns with the research conducted by Stokes et al (44), which demonstrated a higher prevalence of S. aureus in men, particularly in older age groups with comorbidities. Understanding the sex-specific variations in bacterial prevalence holds promise for targeted interventions and tailored awareness campaigns for each sex group (45). By addressing the unique factors influencing UTIs in men and women, progress can be made towards reducing UTI rates and enhancing overall health outcomes (46).
The present investigation into the age distribution of bacterial pathogens revealed significant associations between certain species and different age groups. The study highlighted that Gram-positive bacteria, especially E. faecium, exhibited a marked increase in prevalence among elderly individuals with UTIs. These findings were consistent with those of previous studies (47,48). The notable age-related associations observed for E. coli in the present study demonstrated higher prevalence in younger individuals with UTIs. These age-related patterns of bacterial pathogens add another layer of complexity to our understanding of UTIs. The substantial changes in bacteria prevalence of UTIs with age emphasize the importance of age-specific management strategies leading to better healthcare outcomes (49,50).
The retrospective design, the single tertiary hospital setting, and the lack of detailed information on UTI types are limitations of the present study. Future research with prospective designs and multicenter collaborations through a focused analysis of UTI types is a proactive way to address these limitations and enhance the overall understanding of UTI epidemiology.
In conclusion, the present study provided a comprehensive exploration of UTIs, revealing intricate patterns in bacterial pathogen distribution concerning seasonality, sex, and age. E. coli was the predominant pathogen among UTIs. Significant associations between bacterial species and seasons were observed, with E. faecium prevalent in the spring and A. baumannii in the autumn. Notable sex-specific differences were found in bacterial prevalence, with S. aureus and E. faecalis found more frequently in men. Additionally, age-related associations revealed significant dynamics, with E. faecium exhibiting a marked increase in prevalence with advancing age, while E. coli had a higher prevalence in younger individuals with UTIs. Future research with prospective designs and multicenter collaborations aims to enhance our understanding of UTI epidemiology.
Acknowledgements
Not applicable.
Funding
Funding: Financial support was provided by the Natural Science Foundation Joint Project of Ningde, Ningde, China (grant no. 2022J54).
Availability of data and materials
The data generated in the present study may be requested from the corresponding author upon reasonable request.
Authors' contributions
ZSZhan and JS contributed equally to this work, and were involved in the conception and design of the study, data collection, analysis and interpretation of data, and drafting the manuscript. ZSZheng contributed to the design of the study, data analysis and critically revised the manuscript for important intellectual content. XXZ contributed reagents, materials, analysis tools and data, and analyzed and interpreted the data. JC and XYZ played significant roles in data interpretation, and provided substantial contributions to the manuscript revision. SYZ was responsible for the study concept, analyzed and interpreted the data, wrote and analyzed the methods, and reviewed and edited the manuscript. XXZ and XYZ confirm the authenticity of all the raw data. All the authors read and approved the final manuscript.
Ethics approval and consent to participate
This study was approved by the Medical Ethics Committee of Fuding Hospital, Fujian University of Traditional Chinese Medicine (Fuding, China; approval no. Fuding Hospital 2022325). All methods were conducted according to relevant guidelines and regulations. The requirement for informed consent from participants was waived by the Medical Ethics Committee of Fuding Hospital, Fujian University of Traditional Chinese Medicine, due to the retrospective nature of the study.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
|
Kim DS and Lee JW: Urinary tract infection and microbiome. Diagnostics (Basel). 13(1921)2023.PubMed/NCBI View Article : Google Scholar | |
|
Yang X, Chen H, Zheng Y, Qu S, Wang H and Yi F: Disease burden and long-term trends of urinary tract infections: A worldwide report. Front Public Health. 10(888205)2022.PubMed/NCBI View Article : Google Scholar | |
|
Duicu C, Cozea I, Delean D, Aldea AA and Aldea C: Antibiotic resistance patterns of urinary tract pathogens in children from Central Romania. Exp Ther Med. 22(748)2021.PubMed/NCBI View Article : Google Scholar | |
|
Mancuso G, Midiri A, Gerace E, Marra M, Zummo S and Biondo C: Urinary tract infections: The current scenario and future prospects. Pathogens. 12(623)2023.PubMed/NCBI View Article : Google Scholar | |
|
Chieng CCY, Kong Q, Liou NSY, Khasriya R and Horsley H: The clinical implications of bacterial pathogenesis and mucosal immunity in chronic urinary tract infection. Mucosal Immunol. 16:61–71. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Medina M and Castillo-Pino E: An introduction to the epidemiology and burden of urinary tract infections. Ther Adv Urol. 11(1756287219832172)2019.PubMed/NCBI View Article : Google Scholar | |
|
Öztürk R and Murt A: Epidemiology of urological infections: A global burden. World J Urol. 38:2669–2679. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Simmering JE, Polgreen LA, Cavanaugh JE, Erickson BA, Suneja M and Polgreen PM: Warmer weather and the risk of urinary tract infections in women. J Urol. 205:500–506. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Simmering JE, Cavanaugh JE, Polgreen LA and Polgreen PM: Warmer weather as a risk factor for hospitalisations due to urinary tract infections. Epidemiol Infect. 146:386–393. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Soudais B, Ribeaucoup F and Schuers M: Guidelines for the management of male urinary tract infections in primary care: A lack of international consensus-a systematic review of the literature. Fam Pract. 40:152–175. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Deltourbe L, Lacerda Mariano L, Hreha TN, Hunstad DA and Ingersoll MA: The impact of biological sex on diseases of the urinary tract. Mucosal Immunol. 15:857–866. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Cristina ML, Spagnolo AM, Giribone L, Demartini A and Sartini M: Epidemiology and prevention of healthcare-associated infections in geriatric patients: A narrative review. Int J Environ Res Public Health. 18(5333)2021.PubMed/NCBI View Article : Google Scholar | |
|
Little P, Merriman R, Turner S, Rumsby K, Warner G, Lowes JA, Smith H, Hawke C, Leydon G, Mullee M and Moore MV: Presentation, pattern, and natural course of severe symptoms, and role of antibiotics and antibiotic resistance among patients presenting with suspected uncomplicated urinary tract infection in primary care: Observational study. BMJ. 340(b5633)2010.PubMed/NCBI View Article : Google Scholar | |
|
Gharbi M, Drysdale JH, Lishman H, Goudie R, Molokhia M, Johnson AP, Holmes AH and Aylin P: Antibiotic management of urinary tract infection in elderly patients in primary care and its association with bloodstream infections and all cause mortality: Population based cohort study. BMJ. 364(l525)2019.PubMed/NCBI View Article : Google Scholar | |
|
Goettsch WG, Janknegt R and Herings RMC: Increased treatment failure after 3-days' courses of nitrofurantoin and trimethoprim for urinary tract infections in women: A population-based retrospective cohort study using the PHARMO database. Br J Clin Pharmacol. 58:184–189. 2004.PubMed/NCBI View Article : Google Scholar | |
|
Mengistu DA, Alemu A, Abdukadir AA, Mohammed Husen A, Ahmed F and Mohammed B: Incidence of urinary tract infection among patients: Systematic review and meta-analysis. Inquiry. 60(469580231168746)2023.PubMed/NCBI View Article : Google Scholar | |
|
Huang L, Huang C, Yan Y, Sun L and Li H: Urinary tract infection etiological profiles and antibiotic resistance patterns varied among different age categories: A retrospective study from a tertiary general hospital during a 12-year period. Front Microbiol. 12(813145)2022.PubMed/NCBI View Article : Google Scholar | |
|
Eslami V, Sany SBT, Tehrani H, Ghavami V and Peyman N: Examining health literacy and self-efficacy levels and their association with preventive behaviors of urinary tract infection in Iranian pregnant women: Across sectional study. BMC Womens Health. 23(258)2023.PubMed/NCBI View Article : Google Scholar | |
|
Lean K, Nawaz RF, Jawad S and Vincent C: Reducing urinary tract infections in care homes by improving hydration. BMJ Open Qual. 8(e000563)2019.PubMed/NCBI View Article : Google Scholar | |
|
Prasada Rao CMM, Vennila T, Kosanam S, Ponsudha P, Suriyakrishnaan K, Alarfaj AA, Hirad AH, Sundaram SR, Surendhar PA and Selvam N: Assessment of Bacterial isolates from the urine specimens of urinary tract infected patient. Biomed Res Int. 2022(4088187)2022.PubMed/NCBI View Article : Google Scholar | |
|
Baz AMK, El-Agamy OAE and Ibrahim AM: Incidence of urinary tract infection in neonates with significant indirect Hyperbilirubinemia of unknown etiology: Case-control study. Ital J Pediatr. 47(35)2021.PubMed/NCBI View Article : Google Scholar | |
|
Gajdács M, Bátori Z, Ábrók M, Lázár A and Burián K: Characterization of resistance in gram-negative urinary isolates using existing and novel indicators of clinical relevance: A 10-year data analysis. Life (Basel). 10(16)2020.PubMed/NCBI View Article : Google Scholar | |
|
Lee S and Lee DK: What is the proper way to apply the multiple comparison test? Korean J Anesthesiol. 71:353–360. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Islam MA, Islam MR, Khan R, Amin MB, Rahman M, Hossain MI, Ahmed D, Asaduzzaman M and Riley LW: Prevalence, etiology and antibiotic resistance patterns of community-acquired urinary tract infections in Dhaka, Bangladesh. PLoS One. 17(e0274423)2022.PubMed/NCBI View Article : Google Scholar | |
|
Ullah H, Bashir K, Idrees M, Ullah A, Hassan N, Khan S, Nasir B, Nadeem T, Ahsan H, Khan MI, et al: Phylogenetic analysis and antimicrobial susceptibility profile of uropathogens. PLoS One. 17(e0262952)2022.PubMed/NCBI View Article : Google Scholar | |
|
Shi J, Zhan ZS, Zheng ZS, Zhu XX, Zhou XY and Zhang SY: Correlation of procalcitonin and c-reactive protein levels with pathogen distribution and infection localization in urinary tract infections. Sci Rep. 13(17164)2023.PubMed/NCBI View Article : Google Scholar | |
|
Faine BA, Rech MA, Vakkalanka P, Gross A, Brown C, Harding SJ, Slocum G, Zimmerman D, Zepeski A, Rewitzer S, et al: High prevalence of fluoroquinolone-resistant UTI among US emergency department patients diagnosed with urinary tract infection, 2018-2020. Acad Emerg Med. 29:1096–1105. 2022.PubMed/NCBI View Article : Google Scholar | |
|
FarajzadehSheikh A, Veisi H, Shahin M, Getso M and Farahani A: Frequency of quinolone resistance genes among extended-spectrum β-lactamase (ESBL)-producing Escherichia coli strains isolated from urinary tract infections. Trop Med Health. 47(19)2019.PubMed/NCBI View Article : Google Scholar | |
|
Asadi Karam MR, Habibi M and Bouzari S: Urinary tract infection: Pathogenicity, antibiotic resistance and development of effective vaccines against Uropathogenic Escherichia coli. Mol Immunol. 108:56–67. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Zagaglia C, Ammendolia MG, Maurizi L, Nicoletti M and Longhi C: Urinary tract infections caused by Uropathogenic Escherichia coli strains-new strategies for an old pathogen. Microorganisms. 10(1425)2022.PubMed/NCBI View Article : Google Scholar | |
|
Alrashid S, Ashoor R, Alruhaimi S, Hamed A, Alzahrani S and Al Sayyari A: Urinary tract infection as the diagnosis for admission through the emergency department: Its prevalence, seasonality, diagnostic methods, and diagnostic decisions. Cureus. 14(e27808)2022.PubMed/NCBI View Article : Google Scholar | |
|
Elser H, Rowland ST, Tartof SY, Parks RM, Bruxvoort K, Morello-Frosch R, Robinson SC, Pressman AR, Wei RX and Casey JA: Ambient temperature and risk of urinary tract infection in California: A time-stratified case-crossover study using electronic health records. Environ Int. 165(107303)2022.PubMed/NCBI View Article : Google Scholar | |
|
Rădulescu D, David C, Turcu FL, Spătaru DM, Popescu P and Văcăroiu IA: Combination of cranberry extract and D-mannose-possible enhancer of uropathogen sensitivity to antibiotics in acute therapy of urinary tract infections: Results of a pilot study. Exp Ther Med. 20:3399–3406. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Foxman B: Urinary tract infection syndromes: Occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am. 28:1–13. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Czajkowski K, Broś-Konopielko M and Teliga-Czajkowska J: Urinary tract infection in women. Prz Menopauzalny. 20:40–47. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Silva A, Costa E, Freitas A and Almeida A: Revisiting the frequency and antimicrobial resistance patterns of bacteria implicated in community urinary tract infections. Antibiotics (Basel). 11(768)2022.PubMed/NCBI View Article : Google Scholar | |
|
Magliano E, Grazioli V, Deflorio L, Leuci AI, Mattina R, Romano P and Cocuzza CE: Gender and age-dependent etiology of community-acquired urinary tract infections. ScientificWorldJournal. 2012(349597)2012.PubMed/NCBI View Article : Google Scholar | |
|
Amna MA, Chazan B, Raz R, Edelstein H and Colodner R: Risk factors for non-Escherichia coli community-acquired bacteriuria. Infection. 41:473–477. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Prieto J, Wilson J, Bak A, Denton A, Flores A, Lusardi G, Reid M, Shepherd L, Whittome N and Loveday H: A prevalence survey of patients with indwelling urinary catheters on district nursing caseloads in the United Kingdom: The community urinary catheter management (CCaMa) study. J Infect Prev. 21:129–135. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Shackley DC, Whytock C, Parry G, Clarke L, Vincent C, Harrison A, John A, Provost L and Power M: Variation in the prevalence of urinary catheters: A profile of national health service patients in England. BMJ Open. 7(e013842)2017.PubMed/NCBI View Article : Google Scholar | |
|
Gaston JR, Andersen MJ, Johnson AO, Bair KL, Sullivan CM, Guterman LB, White AN, Brauer AL, Learman BS, Flores-Mireles AL and Armbruster CE: Enterococcus faecalis polymicrobial interactions facilitate biofilm formation, antibiotic recalcitrance, and persistent colonization of the catheterized urinary tract. Pathogens. 9(835)2020.PubMed/NCBI View Article : Google Scholar | |
|
Lara-Isla A, Medina-Polo J, Alonso-Isa M, Benítez-Sala R, Sopeña-Sutil R, Justo-Quintas J, Gil-Moradillo J, González-Padilla DA, García-Rojo E, Passas-Martínez JB and Tejido-Sánchez Á: Urinary infections in patients with catheters in the upper urinary tract: Microbiological study. Urol Int. 98:442–448. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Gajdács M, Ábrók M, Lázár A and Burián K: Increasing relevance of Gram-positive cocci in urinary tract infections: A 10-year analysis of their prevalence and resistance trends. Sci Rep. 10(17658)2020.PubMed/NCBI View Article : Google Scholar | |
|
Stokes W, Parkins MD, Parfitt ECT, Ruiz JC, Mugford G and Gregson DB: Incidence and outcomes of Staphylococcus aureus bacteriuria: A population-based study. Clin Infect Dis. 69:963–969. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Zychlinsky Scharff A, Rousseau M, Lacerda Mariano L, Canton T, Consiglio CR, Albert ML, Fontes M, Duffy D and Ingersoll MA: Sex differences in IL-17 contribute to chronicity in male versus female urinary tract infection. JCI Insight. 5(e122998)2019.PubMed/NCBI View Article : Google Scholar | |
|
Storme O, Tirán Saucedo J, Garcia-Mora A, Dehesa-Dávila M and Naber KG: Risk factors and predisposing conditions for urinary tract infection. Ther Adv Urol. 11(1756287218814382)2019.PubMed/NCBI View Article : Google Scholar | |
|
López-Cruz I, Esparcia A, Madrazo M, Alberola J, Eiros JM and Artero A: Sex differences in aged 80 and over hospitalized patients with community-acquired UTI: A prospective observational study. Heliyon. 8(e11131)2022.PubMed/NCBI View Article : Google Scholar | |
|
Kline KA and Lewis AL: Gram-Positive uropathogens, polymicrobial urinary tract infection, and the emerging microbiota of the urinary tract. Microbiol Spectr. 4(10)2016.PubMed/NCBI View Article : Google Scholar | |
|
Ala-Jaakkola R, Laitila A, Ouwehand AC and Lehtoranta L: Role of D-mannose in urinary tract infections-a narrative review. Nutr J. 21(18)2022.PubMed/NCBI View Article : Google Scholar | |
|
Flores-Mireles AL, Walker JN, Caparon M and Hultgren SJ: Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 13:269–284. 2015.PubMed/NCBI View Article : Google Scholar |
