Saudi Journal of Kidney Diseases and Transplantation

ORIGINAL ARTICLE
Year
: 2020  |  Volume : 31  |  Issue : 5  |  Page : 905--916

Multiple Drug Resistant Urinary Tract Infection in Kidney Transplant Recipients: A Retrospective Cohort Study


Rashid bin Hamid, Shanila Javaid, Muhammad Tassaduq Khan, Naranjan Lal, Shubha Luxmi, Sabahat Sarfaraz 
 Renal Transplant Unit, National Institute of Solid Organ and Tissue Transplantation, Dow University of Health Sciences, Ojha Campus, Karachi, Pakistan

Correspondence Address:
Muhammad Tassaduq Khan
Renal Transplant Unit, National Institute of Solid Organ and Tissue Transplantation, Dow University of Health Sciences, Ojha Campus, Karachi
Pakistan

Abstract

Urinary tract infection (UTI) is the most common infectious disease in post-kidney transplantation patients. The objective of the study was to investigate the prevalence, impact and risk factors of multiple drug resistant (MDR) UTI in kidney transplant recipients. This retrospective cohort study recruited 72 kidney transplant recipients between March 2017 and February 2018. Urine cultures performed during the 1st year of posttransplantation with reference to clinical data were evaluated. Predesigned questionnaire was used to collect data regarding demographic, transplant related, and microbiological information. Multivariate analysis was performed to ascertain risk factors of MDR UTI. Out of 72 patients, 28 (38.9%) had culture guided clinical UTI. Overall, 59 UTI episodes were noted throughout the duration of this study. Eschericia coli were found to be the most frequent uropathogen of UTI among kidney transplant recipients (n = 32, 54.2%). MDR bacteria were responsible for 27.1% (n = 16) of the post-transplantation UTI episodes among patients, with E. coli (n = 9, 56.3%) being the predominant bacterial pathogen. Most of the MDR strains of E. coli (n = 7, 77.8%) were extended spectrum beta-lactamase positive. Female gender (P <0.001), prolonged Foley's catheterization (P = 0.002), coexisting diabetes mellitus (DM) (P <0.001) and induction of anti-thymocyte globulin (ATG) therapy (P <0.001) were independently associated with high risk of MDR UTI. The allograft rejection was found to be significantly higher in patients of posttransplantation UTI with MDR uropathogen (P = 0.009). In conclusion, E. coli were the most prominent uropathogen of UTI with and without MDR pathogen in the present study. Female gender, prolonged Foley's catheterization, coexisting DM, and induction of ATG therapy were the risk factors independently associated with MDR UTI in kidney transplant recipients. MDR organisms were significantly associated with allograft rejection.



How to cite this article:
Hamid Rb, Javaid S, Khan MT, Lal N, Luxmi S, Sarfaraz S. Multiple Drug Resistant Urinary Tract Infection in Kidney Transplant Recipients: A Retrospective Cohort Study.Saudi J Kidney Dis Transpl 2020;31:905-916


How to cite this URL:
Hamid Rb, Javaid S, Khan MT, Lal N, Luxmi S, Sarfaraz S. Multiple Drug Resistant Urinary Tract Infection in Kidney Transplant Recipients: A Retrospective Cohort Study. Saudi J Kidney Dis Transpl [serial online] 2020 [cited 2020 Dec 2 ];31:905-916
Available from: https://www.sjkdt.org/text.asp?2020/31/5/905/301197


Full Text



 Introduction



Kidney transplantation is the ideal remedy for patients with end-stage renal disease (ESRD). A fine balance between immunosuppression and level of immune competency is a precondition to circumvent acute allograft rejection and preserving immunity to avert post-transplantation infection incidence.[1] However, infectious complications are a predominant cause of morbidity and mortality in the kidney transplant patients.[2]

Urinary tract infection (UTI) is classified as the most frequent infectious disease in kidney transplant recipients, with a reported prevalence of approximately 79%.[3],[4],[5],[6],[7] It is responsible for hospitalization in 30% of the kidney transplant recipients.[8] UTI usually develops during early periods of post-transplantation and turns into a less frequent infectious disease after one year of transplantation.[9],[10] A study conducted in Spain demonstrated that 36.5% of the UTI in kidney transplant recipients developed in the 1st month of posttransplantation.[11] The most common risk factors for posttransplantation UTI are old age, female gender, diabetes mellitus (DM), history of vesicoureteral reflux, history of polycystic kidney disease, prolong use of urinary catheter, acute allograft rejection, deceased donor, use of immunosuppressive agents such as mycophenolate mofetil (MMF) or anti-thymocyte globulin (ATG), re-transplantation and delayed allograft function.[9],[12] The UTI may be because of reactivated dormant infection, hospital acquired or emerged de novo infection in the transplant recipient or allograft contamination. It has been suggested that about 20% of the untreated UTI advance toward pyelonephritis, leading to subsequent possibility of lethal urosepsis and allograft loss. Therefore, prompt diagnosis and apposite treatment of UTI are critical for favorable outcomes in kidney transplant patients.[2]

Bacteria are the principal cause of UTI. Fungi and viruses can also result in UTI among kidney transplant recipients; however, UTI triggered by these microorganisms are less prevalent than bacteria.[12] The overriding microorganisms isolated from the kidney transplant recipients producing UTI are Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa and Enterococcus species.[9] However, Gram-negative bacteria are accountable for over 70% of UTI cases; E. coli are the predominant uropathogen. A study conducted in Pakistan by Iqbal et al reported 51% of E. coli isolates from kidney transplant recipients followed by 18% P. aeruginosa.[13] Shams et al also found high prevalence of E. coli (55.3%) uropathogen in kidney transplant recipients of Iran.[1] It has been emphasized that microorganisms that appear in urine culture may not always be pathogens of UTI. For instance, Staphylococcus epidermidis (excluding cases of ureteral stents), Gardnerella vaginalis and Lactobacillus are doubtful to be UTI culprits. Likewise, urine cultures comprising of “mixed flora” (multiple microorganisms) suggest about possible contamination of culture. Mycobacterium tuberculosis, Salmonella species, cytomegalovirus (CMV), and adenovirus are rare pathogens of the urinary tract.[14] BK polyomavirus has recently been found as a significant pathogen in kidney transplant recipients and patients will remain asymptomatic, barring cases with ureteral stenosis. BK polyomavirus related hemorrhagic cystitis is well-recognized in literature in hematopoietic stem cell transplant recipients; however, it is yet to prove in kidney transplant recipients.[15],[16]

With increasing use of antimicrobial drugs in kidney transplant recipients, the incidence of drug-resistant uropathogens is a snowballing menace. In urine cultures of kidney transplant recipients, E. coli were found to be highly trimethoprim-sulfamethoxazole (TMP-SMX) resistant when given for Pneumocystis jiroveci pneumonia prophylaxis in a retrospective study conducted in the Netherlands.[17] Lately, rise of multiple drug resistant (MDR), encompassing extended spectrum beta lactamase (ESBL) or carbapenemase producing microorganisms, has been a worrying situation since it is associated with poor kidney transplant outcomes.[14] A study in Brazil reported progressive increase in incidence, from 13% (1st episode) to 45% (3rd episode), of UTI from ESBL-producing microorganisms in kidney transplant patients.[18] MDR UTI has also been linked with high susceptibility to develop recurrent UTI in kidney transplant patients.[19] A systematic review also revealed that 2–33% kidney transplant recipients developed UTI from an ESBL-producing Enterobacteriaceae.[20] In RESITRA cohort study, the prevalence of ESBL-producing strains was found to be 26.3% among E. coli isolates.[11] Carbapenemresistant Enterobacteriaceae (CRE) is also the emerging microorganism associated with UTI in solid organ transplant recipients.[21] It is identified that CRE accounts for 26% of bacterial infections in kidney transplant patients and urinary tract is the most frequent area of infection.[22],[23] MDR UTI is also accompanied by high frequency of recurrence. Bodro et al evidenced 31% of UTI recurrence due to ESBL-producing K. pneumoniae and 61% of UTI relapse from MDR pathogens.[19] Similarly, UTI by CRE is also linked with a high rate of recurrence.[22],[23]

The dynamics of UTI infection, UTI microorganisms including MDR pathogens and drug susceptibility of those pathogens in kidney transplant recipients have not been explored extensively in Pakistan. Therefore, the objectives of the study were to: (1) Assess the prevalence of MDR UTI in kidney transplant recipients; (2) Identify MDR microorganisms associated with UTI; and (3) Evaluate the impact MDR UTI on allograft function.

 Materials and Methods



Study design and setting

Single center, retrospective cohort research study at Renal Transplant Unit in a tertiary care hospital in Karachi, Pakistan.

Study enrollment duration

March 2017 and February 2018.

Study population

Medical records of adult patients (defined as age ≥18 years) who underwent living donor kidney transplantation, irrespective of previous history of transplantation, were reviewed. Urine cultures performed during 1st year of posttransplantation with reference to clinical data were also evaluated. All the post-transplantation patients had already received Intravenous Piperacillin-Tazobactam (Tanzo) prior to transplant and TMP/SMX on alternate day during the first six month of posttransplant for Pneumocystis pneumonia prophylaxis. Standard transplantation techniques were used for the surgery. Kidney transplant recipients received immunosuppression consisted of prednisolone, cyclosporine, mycophenolate mofetil (MMF), ATG induction and plasmapheresis for focal segmental glomerulosclerosis. ATG was given only to those kidney transplant patients (100 mg/day as induction) with less than three antigen matches or with high PRA; >30% in MHC Class I or Class II. For the prevention of CMV infection and disease, universal prophylaxis with valganciclovir and preemptive therapy were used. MMF dose was reduced accordingly in patients diagnosed with posttransplant UTI. All kidney transplant patients underwent double J stent insertion and were removed six weeks posttransplantation. Kidney transplant recipients who died during the first two days’ posttransplantation, who had missing information, which had followed up in other healthcare organization posttransplantation and who did not followed up at all were excluded from the study. Predesigned questionnaire was used to collect data regarding demographic, transplant related and microbiological information.

Identification of multiple drug resistant/extensive drug resistance urinary tract infection

MDR/extensive drug resistance infections were determined by culture and sensitivity report.

Research ethics

Confidentiality of the subjects was maintained and no personal information that could act as subject identifier was recorded.

Key definition

Asymptomatic bacteriuria: Bacteriuria in a patient without signs and symptoms of UTI.[9] UTI: Bacteriuria in a patient with clinical signs and symptoms (fever, frequency, urgency, dysuria, pyuria, straining, hesitancy, intermittent urinary stream, terminal dribbling, incontinence, incomplete emptying, and nocturia) of urinary tract involvement and quantitative urine bacterial count ≥105 CFU/mL.[9]

Cystitis: Bacteriuria with clinical signs and symptoms of UTI; however, not fulfilling the criteria of pyelonephritis.[9]

Pyelonephritis: Quantitative urine bacterial count ≥ 105 CFU/mL, fever (>38°C) and/or bacteremia with any of the following clinical symptoms: kidney allograft tenderness, costovertebral angle pain, chills and presence of cystitis criteria (bacteriuria and clinical signs and symptoms of fever, frequency, urgency, dysuria and pyuria).[9]

Polymicrobial urinary tract infection: Urine culture confirmed UTI with two or more different microbial organisms.[3]

Early-onset urinary tract infection: Post-transplant UTI within the first six months.[24]

Late-onset urinary tract infection: Post-transplant UTI beyond six months.[3]

Urosepsis: Coexisting positive urine and blood cultures of the identical bacterial strain.[3]

Recurrent UTI: Two consecutive episodes of symptomatic UTI within first six months post-transplantation or three episodes of UTI in 12 months post-transplantation.[2]

UTI Relapse: Recurrent UTI with similar microbial organism.[2]

Reinfection: UTI with different microbial organism.[2]

Delayed kidney allograft function: Need for dialysis within first seven days of post-transplantation.[9]

Acute kidney allograft rejection: Post-transplant serum creatinine >0.3 mg/dL and histological confirmation as per BANFF classification.[25]

UTI associated mortality: Death associated with clinical signs and symptoms of active UTI without other obvious etiology.[3]

MDR: Bacterial organisms resistant to three or more classes of antibiotics.[9]

Extensive drug resistance: Bacterial organisms vulnerable to only one or two classes of antibiotics.[9]

Kidney allograft rejection: Biopsy-confirmed kidney allograft rejection within 12 months posttransplantation as per criteria comprehensively defined in Banff 2013 meeting report.

Kidney allograft loss: Kidney allograft failure needing dialysis or new transplant within 12 months’ posttransplantation.

1-year estimated glomerular filtration rate: The 1-year estimated glomerular filtration rate (eGFR) was computed through the Modification of Diet in Renal Disease formula.

Mortality: All-cause mortality identified within 12 months’ posttransplantation.

Prolonged Foley's catheterization: Foley's catheterization >30 days.[26]

 Statistical Analysis



The IBM SPSS Statistics software version 20.0 (IBM Corp., Armonk, NY, USA) was used to analyze research data. Results are presented as mean ± standard deviation for continuous variables with normal distributions. Student's unpaired t-test or the Mann–Whitney U test was used to compare continuous variables. When appropriate, Pearson's Chi-square test or Fisher's exact test was utilized to compare categorical variables. The threshold of statistical significance was set at P <0.05.

 Results



Baseline profile of kidney transplant recipients

This retrospective cohort study enrolled 73 kidney transplant recipients. One patient was excluded from the study due to ineligibility and hence, 72 kidney transplant recipients were recruited in the final analysis [Figure 1]. The mean age of the subjects was 48.4 ± 6.6 years old. The proportion of female gender was 21 (29.2%). The primary reason for ESRD was found to be kidney disease of glomerular origin; glomerulonephritis (n = 52, 72.2%) followed by diabetic nephropathy (n = 10, 13.9%), IgA nephropathy (n = 7, 9.7%), and adult polycystic kidney disease (n = 3, 4.2%). The average duration of posttransplantation follow-up was 339 ± 125 days. The elaborated demographic and clinical characteristics of study patients are demonstrated in [Table 1].{Figure 1}{Table 1}

Urinary tract infection and microbiological profile in kidney transplant recipients

Out of 72 patients, 28 (38.9%) had culture guided clinical UTI while seven (9.7%) patients had asymptomatic bacteriuria [Figure 1]. In four (14.3%) patients, UTI developed during the 1st month of posttransplantation, in 17 (60.7%) patients excluding those who develop UTI in 1st month, UTI was detected in the first six months after kidney transplantation and in seven (25%) patients, UTI was observed between six and 12 months of posttransplantation. Overall, 59 UTI episodes were noted throughout the duration of this study. Of them, 33 (55.9%) episodes of UTI were categorized as pyelonephritis while 14 (23.7%) episodes were diagnosed as cystitis. Eight (13.6%) episodes of UTI were found to have positive blood culture. A total of 19 (67.9%) patients had single episode of UTI while nine (32.1%) patients had multiple episodes of UTI ranging from two to six. Of 28 posttransplantation patients with UTI, recurrent UTI was observed in five (17.9%) patients, UTI relapse developed in three (10.7%) patients and lastly, only one (3.6%) patient was found to have re-infection UTI episode.

In 59 UTI episodes, E. coli, Gram-negative bacilli was found to be the most frequent uropathogen of UTI among kidney transplant recipients (n = 32, 54.2%), followed by K. pneumoniae, Gram-negative bacilli (n = 17, 28.8%), P. aeruginosa, Gram-negative bacilli (n = 6, 10.2%), Proteus mirabilis, gram-negative bacilli (n = 2, 3.4%), Enterobacter, gram-negative bacilli (n = 1, 1.7%) and Enterococcus fecalis, Gram-positive bacilli (n = 1, 1.7%) [Figure 2]. MDR bacteria were responsible for 27.1% (n = 16) of the post-transplantation UTI episodes among patients, with E. coli (n = 9, 56.3%) being the predominant bacterial pathogen followed by K. pneumoniae (n = 5, 31.2%) and P. aeruginosa (n = 2, 12.5%). Most of the MDR strains of E. coli (n = 7, 77.8%) were ESBL positive while remaining were carbapenem resistant (n = 2, 22.2%). However, all of the MDR strains of K. pneumoniae and P. aeruginosa were carbapenem resistant. No XDR strain was isolated. Polymicrobial infection; more than one microbial pathogen were isolated in eight (13.6%) episodes of UTI. Patient wise distribution of uropathogens isolated from kidney transplant recipients with active UTI according to episodes has been depicted in [Table 2].{Figure 2}{Table 2}

Risk factors for posttransplantation urinary tract infection with multiple drug resistant uropathogen

Through logistic regression analysis, we found following risk factors to be significantly and independently associated with the prevalence of UTI with MDR organism among posttransplant patients in multivariate analysis: female gender [odds ratio (OR) = 1.1, confidence interval (CI) 0.4–5.6, P <0.001]; prolonged Foley's catheterization (OR = 2.6, CI 1.2–5.4, P = 0.002); coexisting DM (OR = 3.4, CI 1.4–6, P <0.001); and induction of ATG therapy (OR = 3.8, CI 1.9–6.7, P <0.001) [Table 3].{Table 3}

Allograft rejection, allograft loss, estimated glomerular filtration rate and mortality at one year in patients of posttransplantation urinary tract infection with and without multiple drug resistant uropathogen

The allograft rejection was found to be significantly higher in patients of posttransplantation UTI with MDR uropathogen than UTI patients without MDR uropathogen (22.2% vs. 5.3%, P = 0.009). The mean eGFR at one year posttransplantation was found to be similar in both the groups;49.4 ± 20.3 in patients of post-transplantation UTI with MDR uropathogen and 52.3 ± 21.5 in patients of post-transplantation UTI without MDR uropathogen (P = 0.062). No mortality and allograft loss at one year posttransplantation was observed in both the cohorts [Table 4].{Table 4}

 Discussion



UTI is by far the most common infectious disease in post kidney transplantation cases.[3] The prevalence of UTI in our study was found to be 38.9% which is very similar to prevalence rates (29%–79%) others have reported in their research studies lately. [3],[4],[5],[6],[7],[27],[28],[29],[30] Our study findings suggested a total of 59 episodes of UTI throughout the duration of this study. Based on the duration of study and number of study participants, the number of UTI episodes could vary from study to study.[2],[3],[8],[9],[30] All the 59 episodes of UTI were observed within the 1st year of kidney transplantation. Similar findings were also conveyed by Mohan et al and other research study.[2],[31] In our study, UTI developed during the 1st month of posttransplantation in 14.3% of the patients, during the first six months in 60.7% of the patients, excluding those who developed UTI in 1st month and between six and 12 months in 25% of the kidney transplant recipients. However, our study findings contrast with that of study conducted by Mohan et al which communicated that most (60%) of the UTI episodes in kidney transplant recipients occurred during the first three months of kidney transplantation.[2] Gołębiewska et al reported 38% of the UTI episodes during the 1st month of kidney transplantation.[32]

Bacteria remain the primary uropathogen of posttransplantation UTI.[2] Our study also found bacteria as the key microorganism triggering UTI in posttransplant patients. No other microorganisms were found to be associated with UTI in our study. E. coli, Gram-negative bacilli, were the most prominent uropathogen in 54.2% of the cases of UTI in our study followed by 28.8% K. pneumoniae, 10.2% P. aeruginosa, 3.4% P. mirabilis, 1.7% Enterobacter and 1.7% E. fecalis. Previous studies have proved E. coli as the key pathogen of posttransplant UTI.[2],[8],[9] MDR bacteria were responsible for 27.1% of the post-transplantation UTI episodes, with E. coli being the predominant bacterial pathogen (15.3%) followed by K. pneumoniae (8.5%). Most of the MDR strains of E. coli were ESBL positive. However, all of the MDR strains of K. pneumoniae were carbapenem resistant. No XDR strain was isolated.

Overall, our study categorized 55.9% of the episodes of UTI as pyelonephritis while 23.7% episodes were diagnosed as cystitis. A study by Freire et al also reported quite comparable findings; 50.9% of pyelonephritis and 17.6% of cystitis cases in patients with posttransplantation UTI episodes.[9] In our study, eight (13.6%) episodes of UTI were found to have positive blood culture. However, Freire et al described significantly high prevalence (23%) of positive blood culture among post-transplant UTI patients.[9] One of the reasons of this discrepancy could be significantly high number of UTI episodes observed in their study due to large sample size and longitudinal nature of the study. Recurrent UTI was observed in 17.9% patients in this study. In comparison past studies have reported very high UTI recurrence rate among kidney transplant recipients; 44% and 46.2%.[2],[33]

Females are more vulnerable to post-transplantation UTI than their male counterparts owing to shorter urethral canal and close proximity to anal opening.[8] In the present study, despite low proportion of females, post-transplant UTI cases were higher in females (64.3%). The most common risk factors associated with posttransplantation UTI are old age, female gender, DM, history of vesicoureteral reflux, history of polycystic kidney disease, prolong use of urinary catheter, acute allograft rejection, deceased donor, use of immunosuppressive agents such as MMF or ATG, re-transplantation, delayed allograft function and prolonged hospital stay.[9],[12],[13],[28],[34],[35] Similarly, studies have mentioned nosocomial infection, female gender and ureteral stenting during kidney transplantation as the key risk factors associated with MDR UTI. In the present study, we found female gender (OR = 1.1, CI 0.4–5.6, P <0.001); prolonged Foley's catheterization (OR = 2.6, CI 1.2–5.4, P = 0.002); coexisting DM (OR = 3.4, CI 1.4–6, P <0.001); and induction of ATG therapy (OR = 3.8, CI 1.9–6.7, P <0.001) as the statistically significant risk factors for MDR UTI on multivariate analysis. Freire et al also found female gender as a risk factor for MDR UTI after multivariate analysis.[9] One main explanation of increased risk of UTI in DM comorbidity is that urine flooded with high glucose levels provides optimal growth medium to uropathogen bacteria.[36] Similarly, extent of immunosuppression could possibly explain induction of ATG therapy as the risk factor of MDR UTI.[1]

In the present study, MDR bacteria were responsible for 27.1% of the post-transplantation UTI episodes. E. coli (56.3%) were the principal bacterial pathogen followed by K. pneumoniae (31.2%) and P. aeruginosa (12.5%). The intracellular camouflage of E. coli protects them from multiple antimicrobial drugs and neutrophils destruction and other host defense systems.[2] A study by Yuan et al reported 62.5% prevalence of E. coli in MDR/XDR cohort of posttransplantation UTI.[3]

However contrasting results have been communicated in literature with several studies reporting K. pneumoniae as the most frequent MDR pathogen of UTI in kidney transplant recipients.[8],[9],[30] Most of the MDR strains of E. coli (77.8%) were ESBL positive while remaining were carbapenem resistant (22.2%). However, all of the MDR strains of K. pneumoniae and P. aeruginosa were carbapenem resistant. We did not discover any strains of XDR bacterial organism. Previous studies have identified carbapenem resistant strains in both E. coli and K. pneumoniae.[2],[9]

The allograft rejection was found to be significantly higher in patients of posttransplantation UTI with MDR uropathogen than UTI patients without MDR uropathogen (P = 0.009). Although the number of rejection cases in UTI with MDR uropathogen group was two and UTI without MDR uropathogen was one; however, all three of them had urosepsis. A study by Ariza-Heredia et al demonstrated that eight out of 15 patients with urosepsis developed kidney allograft rejection within one month of the UTI infection in their study.[37] A study conducted in Pakistan by Iqbal et al reported 35% graft dysfunction among kidney transplant recipients with UTI. They also did not find any graft loss in their study. However, they did not look compare UTI with and without MDR pathogen.[13] The mean eGFR at one year posttransplantation was found to be similar in both the groups (P = 0.062). No mortality and allograft loss at one year posttransplantation was observed in both the cohorts.

This study is not immune to limitations. The single center nature of this research study could hamper the generalizability of our study findings. Healthcare organizations may have different strategies to deal with posttransplantation infections such as antimicrobial prophylaxis which could also limit the application of our results in other healthcare institutions. Hence, we recommend future studies with multicentered study design to validate our research findings and harvest more elaborate results especially in Pakistan.

 Conclusion



In conclusion, we demonstrated that the prevalence of UTI is very high in post-transplantation patients. Female gender was more susceptible to harbor UTI infection. E. coli were the most prominent uropathogen of UTI with and without MDR pathogen in the present study. Female gender, prolonged Foley's catheterization, coexisting DM and induction of ATG therapy were the risk factors independently associated with MDR UTI in kidney transplant recipients. MDR organisms were significantly associated with allograft rejection. The results of the present study highly suggest vigilance in post-transplant infection control measures and appropriate immunosuppression to condense the risk of UTI and subsequent allograft rejection.

Conflict of interest: None declared.

References

1Shams SF, Eidgahi ES, Lotfi Z, et al. Urinary tract infections in kidney transplant recipients 1st year after transplantation. J Res Med Sci 2017;22:20.
2Mohan MV, Neeraja M, Sudhaharan S, Raju SB, Gangadhar T, Lakshmi V. Risk factors for urinary tract infections in renal allograft recipients: Experience of a tertiary care center in Hyderabad, South India. Indian J Nephrol 2017;27:372-6.
3Yuan X, Liu T, Wu D, Wan Q. Epidemiology, susceptibility, and risk factors for acquisition of MDR/XDR Gram-negative bacteria among kidney transplant recipients with urinary tract infections. Infect Drug Resist 2018;11:707-15.
4Leylabadlo HE, Kafil HS, Yousefi M, Aghazadeh M, Asgharzadeh M. Persistent infection with metallo-beta-lactamase and extended spectrum β-lactamase producer Morganella morganii in a patient with urinary tract infection after kidney transplantation. J Nat Sci Biol Med 2016;7:179-81.
5Yabanoğlu H, Alışkan HE, Çalışkan K, et al. Early infections in renal transplant recipients: Incidence, risk factors, and causative microorganisms. Exp Clin Transplant 2015;13 Suppl 3:11-4.
6Espinar MJ, Miranda IM, Costa-de-Oliveira S, Rocha R, Rodrigues AG, Pina-Vaz C. Urinary tract infections in kidney transplant patients due to Escherichia coli and Klebsiella pneumoniae-producing extended-spectrum β-lactamases: Risk factors and molecular epidemiology. PLoS One 2015;10:e0134737.
7Pilmis B, Scemla A, Join-Lambert O, et al. ESBL-producing enterobacteriaceae-related urinary tract infections in kidney transplant recipients: Incidence and risk factors for recurrence. Infect Dis (Lond) 2015;47:714-8.
8Mukherjee D, Sharma S, Nair RK, Datt B, Arora D, Rao A. Urinary tract infection in renal transplant recipients at a tertiary care center in India. Saudi J Kidney Dis Transpl 2018;29:361-8.
9Freire MP, Mendes CV, Piovesan AC, et al. Does the urinary tract infection caused by carbapenem-resistant Gram-negative bacilli impact the outcome of kidney transplant recipients? Transpl Infect Dis 2018;20:e12923.
10Bodro M, Linares L, Chiang D, Moreno A, Cervera C. Managing recurrent urinary tract infections in kidney transplant patients. Expert Rev Anti Infect Ther 2018;16:723-32.
11Vidal E, Torre-Cisneros J, Blanes M, et al. Bacterial urinary tract infection after solid organ transplantation in the RESITRA cohort. Transpl Infect Dis 2012;14:595-603.
12Gondos AS, Al-Moyed KA, Al-Robasi AB, Al-Shamahy HA, Alyousefi NA. Urinary tract infection among renal transplant recipients in Yemen. PLoS One 2015;10:e0144266.
13Iqbal T, Naqvi R, Akhter SF. Frequency of urinary tract infection in renal transplant recipients and effect on graft function. J Pak Med Assoc 2010;60:826-9.
14Goldman JD, Julian K. Urinary tract infections in solid organ transplant recipients: Guidelines from the American society of transplantation infectious diseases community of practice. Clin Transplant 2019;33:e13507.
15Hirsch HH, Randhawa P, AST Infectious Diseases Community of Practice. BK polyomavirus in solid organ transplantation. Am J Transplant 2013;13 Suppl 4:179-88.
16Kamal M, Govil A, Anand M, Abu Jawdeh BG, Shah S. Severe BK polyomavirus-induced hemorrhagic cystitis in a kidney transplant recipient with the absence of renal allograft involvement. Transpl Infect Dis 2018;20: 12814.
17Singh R, Bemelman FJ, Hodiamont CJ, Idu
18MM, Ten Berge IJ, Geerlings SE. The impact of trimethoprim-sulfamethoxazole as Pneumocystis jiroveci pneumonia prophylaxis on the occurrence of asymptomatic bacteriuria and urinary tract infections among renal allograft recipients: A retrospective before-after study. BMC Infect Dis 2016;16:90.
19Pinheiro HS, Mituiassu AM, Carminatti M, Braga AM, Bastos MG. Urinary tract infection caused by extended-spectrum beta-lactamase-producing bacteria in kidney transplant patients. Transplant Proc 2010;42:486-7.
20Bodro M, Sanclemente G, Lipperheide I, et al. Impact of antibiotic resistance on the development of recurrent and relapsing symptomatic urinary tract infection in kidney recipients. Am J Transplant 2015;15:1021-7.
21Alevizakos M, Nasioudis D, Mylonakis E. Urinary tract infections caused by ESBL-producing Enterobacteriaceae in renal transplant recipients: A systematic review and meta-analysis. Transpl Infect Dis 2017;19: 12759.
22Satlin MJ, Jenkins SG, Walsh TJ. The global challenge of carbapenem-resistant Enterobacteriaceae in transplant recipients and patients with hematologic malignancies. Clin Infect Dis 2014;58:1274-83.
23Cicora F, Mos F, Paz M, Allende NG, Roberti J. Infections with blaKPC-2-producing Klebsiella pneumoniae in renal transplant patients: A retrospective study. Transplant Proc 2013;45:3389-93.
24Freire MP, Abdala E, Moura ML, et al. Risk factors and outcome of infections with Klebsiella pneumoniae carbapenemase- producing K. pneumoniae in kidney transplant recipients. Infection 2015;43:315-23.
25Giraldo-Ramírez S, Díaz-Portilla OE, Miranda- Arboleda AF, Henao-Sierra J, Echeverri-Toro LM, Jaimes F. Urinary tract infection leading to hospital admission during the first year after kidney transplantation: A retrospective cohort study. Transplant Rep 2016;1:18-22.
26Loupy A, Haas M, Solez K, et al. The banff 2015 kidney meeting report: Current challenges in rejection classification and prospects for adopting molecular pathology. Am J Transplant 2017;17:28-41.
27Jahn P BK, Langer G. Types of Indwelling Urinary Catheters for Long-term Bladder Drainage in Adults: Cochrane; 2012. Available from: https://www.cochrane.org/CD004997/INCONT_types-of-indwelling-urinary-catheters-for-long-term-bladder-drainage-in-adults.
28Khosravi AD, Abasi Montazeri E, Ghorbani A, Parhizgari N. Bacterial urinary tract infection in renal transplant recipients and their antibiotic resistance pattern: A four-year study. Iran J Microbiol 2014;6:74-8.
29Papasotiriou M, Savvidaki E, Kalliakmani P, et al. Predisposing factors to the development of urinary tract infections in renal transplant recipients and the impact on the long-term graft function. Ren Fail 2011;33:405-10.
30Wu X, Dong Y, Liu Y, et al. The prevalence and predictive factors of urinary tract infection in patients undergoing renal transplantation: A meta-analysis. Am J Infect Control 2016;44:1261-8.
31Silva C, Afonso N, Macário F, Alves R, Mota A. Recurrent urinary tract infections in kidney transplant recipients. Transplant Proc 2013;45: 1092-5.
32Säemann M, Hörl WH. Urinary tract infection in renal transplant recipients. Eur J Clin Invest 2008;38 Suppl 2:58-65.
33Gołębiewska JE, Dębska-Ślizień A, Rutkowski B. Urinary tract infections during the first year after renal transplantation: One center's experience and a review of the literature. Clin Transplant 2014;28:1263-70.
34Camargo LF, Esteves AB, Ulisses LR, Rivelli GG, Mazzali M. Urinary tract infection in renal transplant recipients: Incidence, risk factors, and impact on graft function. Transplant Proc 2014;46:1757-9.
35Menegueti MG, Pereira MF, Bellissimo- Rodrigues F, et al. Study of the risk factors related to acquisition of urinary tract infections in patients submitted to renal transplant. Rev Soc Bras Med Trop 2015;48:285-90.
36Galindo Sacristán P, Pérez Marfil A, Osorio Moratalla JM, et al. Predictive factors of infection in the first year after kidney transplantation. Transplant Proc 2013;45:3620-3.
37Nitzan O, Elias M, Chazan B, Saliba W. Urinary tract infections in patients with Type 2 diabetes mellitus: Review of prevalence, diagnosis, and management. Diabetes Metab Syndr Obes 2015;8:129-36.
38Ariza-Heredia EJ, Beam EN, Lesnick TG, Cosio FG, Kremers WK, Razonable RR. Impact of urinary tract infection on allograft function after kidney transplantation. Clin Transplant 2014;28:683-90.