|Year : 2020 | Volume
| Issue : 4 | Page : 301-308
Clinical profile and risk factors of recurrent urinary tract infection in patients with type 2 diabetes
Consultant, Department of Endocrinology, MMIMSR, Ambala, Haryana, India
|Date of Submission||30-Jun-2020|
|Date of Acceptance||08-Sep-2020|
|Date of Web Publication||24-Dec-2020|
Dr. Tauseef Nabi
E 32, Department of Endocrinology, MMIMSR, Mullana, Ambala, Haryana
Source of Support: None, Conflict of Interest: None
Introduction: Type 2 diabetes (T2D) patients are at increased risk of recurrent urinary tract infection (UTI). The identification of the risk factors can help pinpoint modifiable factors amenable to a disease prevention strategy for recurrent UTI. This study is aimed to find the prevalence, clinical, biochemical profile, and risk factors of recurrent UTI in T2D patients and the effect on glycemic control and renal parameters on follow-up.
Materials and Methods: This was a prospective hospital-based study done on admitted T2D UTI patients. Various clinical, biochemical parameters, and urine examination and culture were monitored. Patients were followed for 6 months concerning the number of UTIs, glycemic control, and renal parameters.
Results: The prevalence of recurrent UTI was 39.6%. Recurrent UTI was common in females 61 (44.8%) compared to males 6 (18.2%). Poor renal function, uncontrolled diabetes, renal calculi, and cystopathy increase the risk of recurrent UTI in T2D females. Whereas in males, poor glycemia and lower estimated glomerular filtration rate (eGFR) increase the risk of recurrent UTI. The recurrent UTI patients had significantly higher glycosylated hemoglobin (HbA1c) at follow-up than at baseline, but renal parameters did not improve despite intensive treatment.
Conclusion: Recurrent UTI is the consequences of uncontrolled glycemia, which in turn perpetuates UTI risk. A significant number of T2D patients develop recurrent UTI on follow-up, especially females. Recurrent UTI causes short and long-term hyperglycemia, and renal function continues to remain altered despite intensive treatment.
The following core competencies are addressed in this article: Medical knowledge, Patient care, Practice-based learning and improvement, and Systems-based practice.
Keywords: Glycemic Control, recurrent urinary tract infection, renal parameters, type 2 diabetes, urinary tract infections
|How to cite this article:|
Nabi T. Clinical profile and risk factors of recurrent urinary tract infection in patients with type 2 diabetes. Int J Acad Med 2020;6:301-8
|How to cite this URL:|
Nabi T. Clinical profile and risk factors of recurrent urinary tract infection in patients with type 2 diabetes. Int J Acad Med [serial online] 2020 [cited 2022 Dec 8];6:301-8. Available from: https://www.ijam-web.org/text.asp?2020/6/4/301/304604
| Introduction|| |
Urinary tract infection (UTI) is an inflammatory response of the urothelium to the bacterial invasion, which is usually free of bacteria. UTI affects women more commonly as compared to men. UTI is a common cause of morbidity and can lead to significant mortality in patients with type 2 diabetes (T2D). The spectrum of UTI ranges from lower UTI (cystitis) to pyelonephritis. Severe complications of UTI, such as emphysematous pyelonephritis (EPN) and emphysematous cystitis, renal abscesses, and renal papillary necrosis, are all encountered frequently in diabetes compared to the general population., The increased risk of UTI globally among patients with diabetes has imposed a substantial burden on medical costs. Besides, the high rates of antibiotic prescription, including broad-spectrum antibiotics, may further induce the development of antibiotic-resistant urinary pathogens.
UTI was found to be 4.1 times more frequent in premenopausal diabetes women than in women without diabetes, in a case–control study of a Washington State health group. A Danish study reported patients with diabetes were three times more likely to be hospitalized with pyelonephritis, as compared to subjects without diabetes.
The traditional definition of recurrent UTI is described as patients having two or more infections in 6 months or having three or more infections in 1 year, and this has been used for studies on risk factors, self-initiated management, and prophylaxis.,,,,, As per the clinical perspective, the second episode of UTI is consideration as a recurrence and requires an approach to diagnosis and management. Majority of these recurrences are thought to be reinfections instead of relapse or failure of initial treatment, although reinfection with the same strain may occur. Modifiable risk factors are very few, and retrospective case–control observational studies suggest that genetic predisposition may play a role.,
Recurrent UTIs are symptomatic infections that follow the complete resolution of a previous UTI. At one primary care setting, 36% of younger women and 53% of women above the age of 55 years report a recurrence within 1 year. Studies on natural history show that 30%–44% of women who have an episode of acute cystitis will suffer a recurrence, mostly within 3 months. Observational cohort studies have found a recurrence rate of 0.3–7.6 infections per patient per year, with an average of 2.6 infections per year., Multiple recurrences often follow an initial infection, resulting in the clustering of episodes. Adult women with diabetes are at increased risk of UTI, especially recurrences.
The clinical presentation of recurrent UTI is similar to sporadic UTI. Symptoms of UTI are similar to patients without diabetes, though some patients with diabetic neuropathy may have altered clinical signs. Factors responsible to increase the risk for UTI in patients of diabetes include metabolic control, age, and long-lasting complications, primarily diabetic nephropathy and cystopathy.
The pathogenesis of recurrent UTI is the same as of sporadic infection, and 68%–77% of recurrences caused by Escherichia coli involve strains genetically indistinguishable from those that caused previous infections. The most common pathogens isolated from the urine of T2D with UTI are E. coli, other Enterobacteriaceae. Diabetic patients are prone to have resistant pathogens as the cause of their UTI. Follow-up studies are showing that the same E. coli strain can cause recurrence after 1–3 years, even with negative urine cultures in between the initial infection and the recurrence.
Higher concentrations of glucose in the urine may promote the growth of pathogenic bacteria. The pathogenesis of UTI in diabetic patients is also contributed by impairment in the immune system, including innate, humoral, and cellular immunity. Autonomic neuropathy, which involves the genitourinary tract, results in urinary retention and dysfunctional voiding, decreasing physical bacterial clearance through micturition, eventually facilitating bacterial growth.
Recurrent UTIs are common phenomena amongst pre- and post-menopausal women. Patients with recurrences must be recognized through a proper history and examination. Risk factors should be identified and addressed accordingly; antibiotics remain the most effective method of management. However, the studies concerning the association between recurrent UTI and diabetes characteristics, such as glycemic control and vascular complications, are scarce. Therefore, with this study, we intend to look at the prevalence, clinical, biochemical profile, and risk factors of recurrent UTI in patients with T2D. The hypothesis was that poor glycemic control predisposes to recurrent UTI, which in turn cause renal impairment. The identification of risk factors can help pinpoint modifiable factors amenable to a disease prevention strategy.
| Materials and Methods|| |
This was a prospective study was a prospective hospital-based study of adult T2D patients attending the tertiary care hospital in North India. Ethical clearance was taken from the institutional ethical committee. Informed consent was obtained from all the participants.
The study recruited consecutive two hundred UTI patients admitted in the Endocrinology Department, and they were followed for 6 months. This study was conducted over a period of 2½ years from January 2016 to June 2018. The research was conducted following the Declaration of Helsinki. All patients were interviewed at baseline using a standardized questionnaire regarding the number of UTIs within the previous year and the treatment for the same, urinary tract surgery, marital status, and menopausal status in females. A detailed physical examination of the subjects was carried based on a study protocol. The eligibility criteria for including the subject in the study were: both male and female T2D patients having age >30 years. The exclusion criteria were: (i) Type 1 diabetes, (ii) Gestational diabetes, (iii) Immunocompromised states-HIV, malignancy, patients on steroids and transplant recipients, (iv) Recent hospitalization/surgery, (v) Use of antimicrobial drugs within the previous 14 days, (vi) Patients on prophylaxis for recurrent UTI, and (vii) Urinary tract surgery/instrumentation.
Detailed study design
Clinical and biochemical parameters
Clinical parameters including duration and complications of diabetes, drug therapy, clinical symptomatology, especially urinary complaints (fever, dysuria, hematuria, increased frequency, nausea/vomiting, flank pain, altered sensorium, and renal tenderness) and comorbidities (hypertension [HTN], obesity, hypothyroidism, chronic kidney disease [CKD], coronary artery disease [CAD] and others) were recorded. Patients were followed for 6 months with regard to the number of UTIs (urine examination or culture documented) and any treatment received for the same. Complete blood count (CBC), renal function test (KFT), fasting blood glucose (FBG), and 2-h postprandial blood glucose (PP), 24-h urinary protein estimation, and glycosylated hemoglobin (HbA1c) was estimated at baseline and at 6 months. HbA1c was measured by column chromatography (Bio-Rad, Richmond, CA) with whole blood collected in EDTA. Ultrasonography (USG) of the abdomen was done in all admitted patients. Blood culture and noncontrast computed tomography abdomen were done as per requirement.
Urine examination and culture sensitivity
Voided, clean-catch, and midstream urine samples were collected from patients in a sterile wide-mouth container for routine urine analysis and culture sensibility at baseline and at 6 months. The study participants were educated on how to collect a “clean-catch” midstream urine specimen and the importance to avoid contamination. Samples were inoculated on Hichrome UTI agar media. The organisms were identified using standard cultural, morphological, and biochemical techniques. UTI patients were divided into lower UTI (cystitis) who had dysuria, frequency of urination, urgency, and/or abdominal discomfort. Upper UTI (pyelonephritis) was said to be present when the patient complained of fever (>38.3°C) with chills and rigors, flank pain, nausea, and vomiting and USG was suggestive of a combination of enlarged kidney, presence of collection and/or perinephric stranding and EPN when imaging showed characteristic features of same. Recurrent UTI was defined when a new episode of UTI occurred after 2 weeks of symptom-free period from index UTI episode at study entry.
Pyuria (defined as ≥10 leukocytes/mm3) and hematuria (defined as ≥3 red blood cell/hpf) were detected by microscopic examination. For the diagnosis of significant bacteriuria in women, a midstream urine count ≥105 colony-forming unit (CFU/ml) was considered diagnostic. Whereas for the diagnosis of bacteriuria in men, a midstream urine colony count of ≥104 CFU/ml was indicative. When the growth of 3 or more different microorganisms was seen, the urine specimen was considered to be contaminated. Obesity was defined as body mass index ≥25 kg/m2 as per Asian Indian criteria; uncontrolled HTN was defined as systolic blood pressure of ≥140 or diastolic blood pressure of ≥90 mmHg, diabetes control when HbA1c <7%, and uncontrolled when HbA1c ≥7%, proteinuria was defined as 24-h urinary protein ≥150 mg, glycosuria was defined as the presence of glucose in the urine, acute kidney injury (AKI) when creatinine increased by 0.3 mg/dl from baseline or absolute value ≥1.5 mg/dl after excluding CKD, and leukocytosis as total leukocyte count more than the upper normal limit for the laboratory (4–10 × 103/μL). Cystopathy, when the patient has decreased bladder sensation, and post-void residual urine was >150 ml. Prostatomegaly was defined when the prostate gland ≥30 g in size on USG. The estimated glomerular filtration rate (eGFR) was calculated by CKD-EPI(CKD epidemiology collaboration).
The recommended duration of antibiotic treatment for UTI in diabetes was followed, and patients who had two UTI episodes after study entry received continuous oral antibiotic prophylaxis for 3 months as per culture sensitivity.
UTI patients were followed for 6 months for the number of UTIs (urine examination or culture documented), any antibiotic treatment received for the same and hospitalizations. At the end of follow-up, these patients again underwent urine examination, urine culture sensitivity, 24-h urinary protein estimation, FBG, PP, CBC, KFT, and HbA1c.
Quantitative variables were presented as means ± standard deviation, while qualitative variables were expressed in terms of proportion. Descriptive and univariate analytic techniques were used to analyze the data. Categorical variables were compared employing Chi-square test and Fisher's exact tests, whereas continuous variables were compared by using Student's t-test for independent observations. For paired or matched observations, McNemar's test and paired Student's t-test were used for categorical and continuous variables, respectively. To study the joint effects and interactions of various independent variables, binary logistic regression analysis was carried out to calculate multivariate P-value. Out of 169 patients followed for 6 months, 67 patients developed recurrent UTI, which were compared for risk. P < 0.05 were considered statistically significant. All the analyses were performed using statistical software SPSS Version 21 (IBM SPSS Statistics for Windows, version 21 Armonk, NY, USA: IBM Corp.).
| Results|| |
Of the 200 UTI patients, only 169 had completed follow-up at 6 months. 67 (39.6%) developed recurrent UTI, 33 patients developed one episode, 20 patients, two episodes, 10 patients, three episodes, 3 patients four episodes, and 1 patient five episodes. [Table 1] demonstrates the risk factors for recurrent UTI in T2D women. Out of 136 T2D female patients with UTI who were followed for 6 months, 61 (44.8%) patients again developed UTI during follow-up with 109 episodes of UTI. The frequency of UTI was that 32 patients developed one episode, 15 patients two episodes, 10 patients three episodes, 3 patients four episodes, and 1 patient five episodes. Thirty-one episodes were pyelonephritis, whereas rest were lower UTI and all episodes received antibiotic treatment. Various factors such as age, marital status, and postmenopausal state, did not significantly correlate, whereas longer diabetes duration was significantly (P = 0.012) associated with the development of recurrent UTI on follow-up. With regard to diabetic microvascular complications, retinopathy, and nephropathy were significantly (P = 0.002) associated with the development of recurrent UTI.
|Table 1: Risk factors for the recurrent urinary tract infection in type 2 diabetes women with urinary tract infection|
Click here to view
With regard to comorbidities (such as HTN, hypothyroidism, CKD, CAD, and dyslipidemia), only CKD was associated with the development of a recurrent UTI on follow-up (P = 0.001). HbA1c was significantly (P = 0.001) associated with recurrent UTI. Renal parameters (serum creatinine and eGFR) and proteinuria also were significantly associated with recurrent UTI (P < 0.05). Renal calculi and cystopathy did predict the development of recurrent UTI in T2D female patients. On multivariate analysis, the factors which were found to correlate with recurrent UTI on follow-up in T2D female patients were a presence of CKD, renal calculi, cystopathy, lower eGFR and higher HbA1c.
[Table 2] demonstrates the risk factors for the recurrent UTI in a T2D male. Out of 33 T2D male patients with UTI who were followed for 6 months, 6 (18.2%) patients again developed UTI during follow-up with 11 episodes of UTI. The frequency of UTI was that 1 patient developed one episode and 5 patients two episodes. 6 episodes were pyelonephritis whereas rest were lower UTI, and all episodes received antibiotic treatment. Various factors such as age, diabetes duration, type of antidiabetic treatment, diabetic microvascular complication and UTI in the previous 1 year did not significantly increase the risk of recurrent UTI on follow-up in T2D male patients. With regard to comorbidities, only CKD was associated with the development of a recurrent UTI (P = 0.0.22). FBG (P = 0.043) and HbA1c (P = 0.009) were significantly associated with recurrent UTI. Poor renal function and proteinuria were significantly associated with recurrent UTI (P < 0.05). Prostatomegaly predicted recurrent UTI (P = 0.043). On multivariate analysis, the factors which were found to correlate with recurrent UTI in T2D male patients were lower eGFR and higher HbA1c.
|Table 2: Risk factors for the recurrent in type 2 diabetes men with urinary tract infection|
Click here to view
[Table 3] reveals the comparison of baseline and follow-up parameters of 169 UTI patients. UTI T2D patients with recurrent UTI (67 patients) had significantly higher HbA1c at follow-up (12.56% ± 0.82%) than at baseline (11.73% ± 2.42%) (P = 0.012). Renal parameters and proteinuria did not significantly improve at follow-up (P < 0.05). Mean FBG and blood glucose PP reduced at follow-up from baseline in T2D patients with nonrecurrent UTI (102 patients) (P < 0.001), but HbA1c insignificantly (P = 0.729) changed from 10.34% ± 1.85% to 10.27% ± 1.03% at follow-up. eGFR increased insignificantly (P = 0.114) at follow-up. Renal function improved at follow-up in nonrecurrent UTI patients.
|Table 3: Follow-up of type 2 diabetes patients with urinary tract infection based on recurrent urinary tract infection|
Click here to view
| Discussion|| |
T2D patients are at increased risk of infections, with the urinary tract being the most frequent site. and good diabetic control will decrease this risk. UTIs in T2D are a common cause of morbidity and can lead to mortality. UTI in patients with diabetes is often given less importance, more attention being paid to other chronic complications of diabetes. Recurrent UTIs are common phenomena amongst T2D patients. Patients with recurrences must be recognized through a thorough history and examination. The identification of the risk factors can help pinpoint modifiable factors amenable to a disease prevention strategy. Therefore, in this study, we have calculated the prevalence, clinical and risk factors of recurrent UTI in T2D patients and effect on glycemic control and renal parameters on follow-up.
Prevalence, clinical profile and risk factors of recurrent urinary tract infection
In our study, the prevalence of recurrent UTI in T2D patients was 39.6%, with 44.8% in females as compared to 18.2% in males. Various factors like the presence of CKD, renal calculi, cystopathy, lower eGFR and higher HbA1c were significantly associated with the development of recurrent UTI in female T2D patients. At the same time, age, postmenopausal state, longer diabetes duration and diabetic microvascular complications did not influence the development of recurrent UTI in our study, as shown in [Table 1]. While in male patients, recurrent UTI correlates with lower eGFR and higher HbA1c. The study has shown over one-fourth of patients have a second infection within 6 months. In the study conducted by Gorter, et al. relapses and reinfections were reported in 7.1% and 15.9% of diabetic women. In a Finnish study of women ages 17–82 who had E. coli cystitis, 44% had a recurrence within 1 year. Recurrent UTI was common in postmenopausal female in the Finnish study, but it was not statistically significant, but another study has shown considerable association. Gorter, et al. showed a more prolonged duration of diabetes and retinopathy were associated with recurrent UTI in diabetic females. Hyperglycemia in poorly controlled diabetes acts as a favorable environment for bacterial growth predisposing to recurrent UTI. Renal calculi also act as a nidus for bacteria, hence causing recurrent UTI. To prevent this, renal calculi should be addressed aggressively. Cystopathy causes stagnation of urine in the bladder, which serves as a source for bacterial growth.
Follow-up of type 2 diabetes patients with urinary tract infection
In our study, recurrent UTI patients had significantly higher HbA1c at follow-up (12.56% ± 0.82%) than at baseline (11.73% ± 2.42%). Renal parameters and proteinuria did not worsen at follow-up, as shown in [Table 3]. This denotes that recurrent UTI causes short- and long-term hyperglycemia and renal function continues to remain altered despite a large number of patients had AKI even with intensive treatment. Recurrent UTI is the consequence of or leads to uncontrolled glycemia and perpetuates UTI risk. There are lack of studies which have followed recurrent UTI patients with T2D for glycemic and renal effect.
E. coli was still the most common cause of recurrence while another study also revealed E. coli is not only the number one cause of UTI in women, but it also increases the likelihood of recurrent UTI.
This study needs to be considered in light of strengths and limitations. Prospective nature and adequate sample size were some of the strengths of the study. The present study had several limitations. First, it was a single-center study; second, other risk factors like frequency of sexual intercourse and the use of condoms were not analyzed, which are the risk factors for recurrent UTI, and the duration of follow-up of study participants was short. Third, the detailed management of recurrent UTI has not been discussed in this article.
| Conclusion|| |
Recurrent UTI is consequence of uncontrolled glycemia, which in turn perpetuates UTI risk. A significant number of T2D patients develop recurrent UTI on follow-up, especially females. Recurrent UTI causes short- and long-term hyperglycemia, and renal function continues to remain altered despite intensive treatment. Long-term prospective studies on recurrent UTI in T2D patients are required to identify risk factors which can help pinpoint modifiable factors amenable to a disease prevention strategy and improve the overall management.
The authors would like to express their greatest gratitude to all participating patients, health professionals and community support group members who provided assistance for this study. I am thankful to Dr. Nayeem U Din Wani, Lecturer Microbiology, for helping in the interpretation of the urine culture and Dr. Hifz Ur Rahman for helping me in the statistical analysis of the data. I also thank the technical department of the microbiology of the institute.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
Ethical conduct of research
Appropriate approval was obtained from institutional ethics committee (number IEC/SKIMS/2015-235 dated December 31, 2015). Clinical trials registration was not done as it was observational study. The authors declare that they followed applicable EQUATOR Network (http://www.equator-network.org/) research reporting guidelines.
| References|| |
Kofteridis DP, Papadimitraki E, Mantadakis E, Maraki S, Papadakis JA, Tzifa G, et al
. Effect of diabetes mellitus on the clinical and microbiological features of hospitalized elderly patients with acute pyelonephritis. J Am Geriatr Soc 2009;57:2125-8.
Mnif MF, Kamoun M, Kacem FH, Bouaziz Z, Charfi N, Mnif F, et al
. Complicated urinary tract infections associated with diabetes mellitus: Pathogenesis, diagnosis and management. Indian J Endocrinol Metab 2013;17:442-5.
Yu S, Fu AZ, Qiu Y, Engel SS, Shankar R, Brodovicz KG, et al
. Disease burden of urinary tract infections among type 2 diabetes mellitus patients in the U.S. J Diabetes Complications 2014;28:621-6.
Venmans LM, Hak E, Gorter KJ, Rutten GE. Incidence and antibiotic prescription rates for common infections in patients with diabetes in primary care over the years 1995 to 2003. Int J Infect Dis 2009;13:e344-51.
Scholes D, Hooton TM, Roberts PL, Gupta K, Stapleton AE, Stamm WE. Risk factors associated with acute pyelonephritis in healthy women. Ann Intern Med 2005;142:20-7.
Benfield T, Jensen JS, Nordestgaard BG. Influence of diabetes and hyperglycaemia on infectious disease hospitalisation and outcome. Diabetologia 2007;50:549-54.
Albert X, Huertas I, Pereiró II, Sanfélix J, Gosalbes V, Perrota C. Antibiotics for preventing recurrent urinary tract infection in non-pregnant women. Cochrane Database Syst Rev 2004;3:CD001209.
Fihn SD. Clinical practice. Acute uncomplicated urinary tract infection in women. N Engl J Med 2003;349:259-66.
Gupta K, Hooton TM, Roberts PL, Stamm WE. Patient-initiated treatment of uncomplicated recurrent urinary tract infections in young women. Ann Intern Med 2001;135:9-16.
Scholes D, Hooton TM, Roberts PL, Stapleton AE, Gupta K, Stamm WE. Risk factors for recurrent urinary tract infection in young women. J Infect Dis 2000;182:1177-82.
Stapleton A. Prevention of recurrent urinary-tract infections in women. Lancet 1999;353:7-8.
Stapleton A, Latham RH, Johnson C, Stamm WE. Postcoital antimicrobial prophylaxis for recurrent urinary tract infection. A randomized, double-blind, placebo-controlled trial. JAMA 1990;264:703-6.
Hawn TR, Scholes D, Li SS, Wang H, Yang Y, Roberts PL, et al
. Toll-like receptor polymorphisms and susceptibility to urinary tract infections in adult women. PLoS One 2009;4:e5990.
Scholes D, Hawn TR, Roberts PL, Li SS, Stapleton AE, Zhao LP, et al
. Family history and risk of recurrent cystitis and pyelonephritis in women. J Urol 2010;184:564-9.
Hooton TM. Recurrent urinary tract infection in women. Int J Antimicrob Agents 2001;17:259-68.
Ikäheimo R, Siitonen A, Heiskanen T, Kärkkäinen U, Kuosmanen P, Lipponen P, et al
. Recurrence of urinary tract infection in a primary care setting: Analysis of a 1-year follow-up of 179 women. Clin Infect Dis 1996;22:91-9.
Foxman B. Epidemiology of urinary tract infections: Incidence, morbidity, and economic costs. Am J Med 2002;113 Suppl 1A:5S-13S.
Stamm WE, McKevitt M, Roberts PL, White NJ. Natural history of recurrent urinary tract infections in women. Rev Infect Dis 1991;13:77-84.
Muller LM, Gorter KJ, Hak E, Goudzwaard WL, Schellevis FG, Hoepelman AI, et al
. Increased risk of common infections in patients with type 1 and type 2 diabetes mellitus. Clin Infect Dis 2005;41:281-8.
Brown JS, Wessells H, Chancellor MB, Howards SS, Stamm WE, Stapleton AE, et al
. Urologic complications of diabetes. Diabetes Care 2005;28:177-85.
Russo TA, Stapleton A, Wenderoth S, Hooton TM, Stamm WE. Chromosomal restriction fragment length polymorphism analysis of Escherichia coli
strains causing recurrent urinary tract infections in young women. J Infect Dis 1995;172:440-5.
Geerlings SE, Meiland R, van Lith EC, Brouwer EC, Gaastra W, Hoepelman AI. Adherence of type 1-fimbriated Escherichia coli
to uroepithelial cells: More in diabetic women than in control subjects. Diabetes Care 2002;25:1405-9.
Ejrnæs K, Stegger M, Reisner A, Ferry S, Monsen T, Holm SE, et al
. Characteristics of Escherichia coli
causing persistence or relapse of urinary tract infections: Phylogenetic groups, virulence factors and biofilm formation. Virulence 2011;2:528-37.
Fünfstück R, Nicolle LE, Hanefeld M, Naber KG. Urinary tract infection in patients with diabetes mellitus. Clin Nephrol 2012;77:40-8.
Delamaire M, Maugendre D, Moreno M, Le Goff MC, Allannic H, Genetet B. Impaired leucocyte functions in diabetic patients. Diabet Med 1997;14:29-34.
Kaplan SA, Te AE, Blaivas JG, McGuire EJ. Urodynamic findings in patients with diabetic cystopathy. J Urol 1995;153:342-4.
Gorter KJ, Hak E, Zuithoff NP, Hoepelman AI, Rutten GE. Risk of recurrent acute lower urinary tract infections and prescription pattern of antibiotics in women with and without diabetes in primary care. Fam Pract 2010;27:379-85.
Bucchanan R, Gibbons M. Bergey's Manual of Determinative Bacteriology. 8th
ed. Baltimore, USA: Williams & Wilkins Baltimaore; 1974.
Rubin RH, Shapiro ED, Andriole VT, Davis RJ, Stamm WE. Evaluation of new anti-infective drugs for the treatment of urinary tract infection. Infectious Diseases Society of America and the Food and Drug Administration. Clin Infect Dis 1992;15 Suppl 1:S216-27.
Kass EH. Asymptomatic infections of the urinary tract. J Urol 2002;167:1016-20.
Joshi N, Caputo GM, Weitekamp MR, Karchmer AW. Infections in patients with diabetes mellitus. N Engl J Med 1999;341:1906-12.
Bagdade JD. Infection in diabetes, predisposing factors. Postgrad Med 1976;59:160-4.
Foxman B. Recurring urinary tract infection: Incidence and risk factors. Am J Public Health 1990;80:331-3.
Raz R, Gennesin Y, Wasser J, Stoler Z, Rosenfeld S, Rottensterich E, et al
. Recurrent urinary tract infections in postmenopausal women. Clin Infect Dis 2000;30:152-6.
Foxman B, Gillespie B, Koopman J, Zhang L, Palin K, Tallman P, et al
. Risk factors for second urinary tract infection among college women. Am J Epidemiol 2000;151:1194-205.
[Table 1], [Table 2], [Table 3]