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Table of Contents
Year : 2020  |  Volume : 14  |  Issue : 2  |  Page : 104-110

Clinical profile and predisposing factors for the development of urinary tract infection during the first 3 months postrenal transplantation: A tertiary care hospital experience

1 Department of Nephrology, Institute of Renal Science, Sir Gangaram Hospital, New Delhi, India
2 Department of Microbiology, Sir Gangaram Hospital, New Delhi, India

Date of Submission14-Nov-2019
Date of Acceptance13-Apr-2020
Date of Web Publication06-Jul-2020

Correspondence Address:
Dr. Priti Meena
Institute of Renal Science, Sir Gangaram Hospital, New Delhi - 110 092
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijot.ijot_66_19

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Background: Infections in renal allograft recipients, especially urinary tract infections (UTI), are an essential factor leading to an increase in morbidity, graft failure, and degrading the health-related quality of life. Aims and Objectives: Our objective is to assess the causes, risk factors, microbiological profile, and antibiotic sensitivity pattern of UTI in renal transplant recipients. Material and Methods: It was a prospective observational study, conducted at the Department of Nephrology, Sir Gangaram Hospital, New Delhi, India. Three hundred ten renal transplant recipients were enrolled. Results: Out of 300 transplant recipients, 107 (35.6%) had UTI. The mean age of patients with UTI was 32 ± 10.5 years. Females have a higher incidence of UTI than males. 64.5% of all diabetic patients had UTI. Escherichia coli (41%) was the most common causative agent. Gram-negative bacilli attributed the majority (88.5%) of cases. Klebsiella pneumonia was found to be multidrug-resistant in most cases. 61% of patients with reflux kidney disease before transplant suffered from UTI. Conclusion: On multivariate analysis in our study, diabetes (P=0.01), prolonged urethral catheterization (p=0.002), and double J stent kept in situ (p=0.03) and reflux kidney disease before transplant (p < 0.02) were independently associated with UTI prolonged.

Keywords: Antibiotic resistance, asymptomatic bacteriuria, end-stage renal disease, reflux nephropathy, renal transplant, urinary tract infection

How to cite this article:
Meena P, Rana DS, Bhalla AK, Gupta A, Malik M, Gupta A, Bhargava V, Tiwari V, Wattal C. Clinical profile and predisposing factors for the development of urinary tract infection during the first 3 months postrenal transplantation: A tertiary care hospital experience. Indian J Transplant 2020;14:104-10

How to cite this URL:
Meena P, Rana DS, Bhalla AK, Gupta A, Malik M, Gupta A, Bhargava V, Tiwari V, Wattal C. Clinical profile and predisposing factors for the development of urinary tract infection during the first 3 months postrenal transplantation: A tertiary care hospital experience. Indian J Transplant [serial online] 2020 [cited 2022 Oct 5];14:104-10. Available from: https://www.ijtonline.in/text.asp?2020/14/2/104/289051

  Introduction Top

Since 1950 when the first renal transplantation was done, knowledge in various aspects, affecting the graft survival and result, is progressively escalating. However, infections, especially urinary tract infections, are an essential factor leading to an increase in morbidity and graft failure.[1] UTI (urinary tract infection) deteriorates the health-related standard of living and can potentially impair graft function. UTI occurs in 25 percent of kidney transplant recipients within one year of transplant and responsible for 44-47 percent of all infectious complications.[2] Asymptomatic bacteriuria, uncomplicated UTI, and complicated UTI comprise 44, 32, and 24 percent of cases, respectively.[3] In our study, we analyzed the incidence of UTI within the first three months post-renal transplant, its predisposing factors, causative microorganisms, and their antibiotic resistance pattern. The main aim of our study was to identify the risk factors and antibiotic resistance of the organisms that would help in coping with the multidrug-resistant infection.

  Materials and Methods Top

We performed a prospective observational study on all the patients of age > 18 years who had undergone renal transplant surgery during the study period of 1 year from January 2018 to December 2018 at a tertiary care hospital (Sir Ganga Ram Hospital, New Delhi). Our study had recruited a total of 310 patients. Eight patients were lost to follow-up, and two patients died during the study period. Possible risk factors for urinary tract infections (UTI) development such as diabetes, history of UTI before renal transplant, urinary tract abnormality and, history of recent instrumentation were recorded. Clinical symptoms such as fever, dysuria, graft site pain, increased urinary frequency, and hematuria were recorded from all the patients. Fresh voiding morning mid-stream clean-catch urine samples were obtained for culture and routine microscopy. The urine specimen was transported within 2 h to the microbiology laboratory. For patients using urinary catheters, urine was aseptically obtained by sampling through the catheter port using the sterile technique or, if a port was not present, puncturing the catheter tubing with a needle and syringe. In patients with long-term indwelling catheters, urine specimen was taken from a freshly placed catheter. An initial urine sample was taken 2 days prior to transplantation except in anuric patients. Urine routine microscopy and urine culture and sensitivity were performed for all the patients. Urine samples were inoculated onto a MacConkey agar plate for quantitative culture and incubated at 37°C for 48 h. The bacterial strains were shown up using a semi automated VITEK 2 system (Biomérieux- usa), uses Advanced Colorimetry™, for bacteria and yeast identification (ID) and antibiotic susceptibility testing (AST). it has bi-directional interface and ADVANCED EXPERT SYSTEM™ (AES) software for on-line result validation, which was also used for evaluating sensitivity to antimicrobial agents, according to the criteria of the Clinical Laboratory Standards Institute. Urine microscopy and urine cultures were performed every 3 days within the first 12 days after renal transplantation and then during follow-up outpatient visits first, at 1 week after discharge, and later on outpatient visits in the 2nd and 3rd months. Screening for CMV infection and BK virus is not in the protocol of our hospital, so they were done only in case of clinical suspicion. Imaging such as ultrasonography and computed tomography scan of graft or native kidney and urinary bladder was done if required.

The patient consent has been taken for participation in the study and for publication of clinical details and images. Patients understand that the names, initials would not be published, and all standard protocols will be followed to conceal their identity. The study has been approved by Institutional Board Review, Ethical Committee, Sir Ganga Ram Hospital New Delhi (EC/07/17/1195).

Antibiotic prophylaxis protocol

All patients received intravenous cefuroxime sodium 1.5 g single dose perioperatively; it was continued with a dose of 1.5 g twice daily, usually for 7 days posttransplant. All patients have received 80/400 mg of trimethoprim/sulfamethoxazole daily for 6 months.

Protocol for double-J ureteral stent and urethral catheter

The decision to place a double-J ureteral stent was surgeon dependent, and it was inserted routinely in all the patients. A urethral catheter was inserted in each patient preoperatively and removed between the 6th and 8th days posttransplantation, while the double-J ureteral stent was removed after 4–6 weeks (as a protocol at our center) from posttransplantation.

Immunosuppression protocol

All patients were given tacrolimus (0.15 mg/kg/day in two divided doses), and mycophenolate mofetil (MMF) 1 g twice a day, started 2 days before renal transplant surgery. Preoperatively (day 0) induction with monoclonal (basiliximab) or polyclonal antibodies (ATG) was given in some patients according to the immunological risk of the patients. Methylprednisolone was used in all patients. Post transplant, they were maintained on a triple-drug regimen. The most common regimen used included tacrolimus + MMF/sodium + glucocorticosteroids. Other combinations of immunosuppression included cyclosporine/prednisolone/MMF/sodium (MPS). A few other patients were given a combination of prednisolone, tacrolimus 0.15 mg/kg/day in divided doses, and everolimus.

Definitions of urinary tract infections

An episode of UTI was considered if at least one of the following symptoms or signs were present: fever (>38°C); costovertebral angle pain or tenderness; and suprapubic pain or a positive urine culture of ≥105 colony-forming units (CFU)/mL with no more than two species of microorganisms.

UTIs are also diagnosed in patients with fever (>38°C), urgency, frequency, dysuria, suprapubic tenderness, costovertebral angle pain or tenderness, and at least one of the following results: (a) pyuria (urine specimen with ≥10 white blood cells (WBC)/mm 3 of unspun urine or > 5 WBC/high-power field of spun urine; or (b) microorganisms observed on Gram's stain of unspun urine and a positive urine culture of ≥103 and <105 CFU/mL with no more than two species of organisms.

Patients with fever (with or without flank/allograft pain) and a urine culture positive for urinary tract pathogens (104 CFU/mL) were diagnosed as having acute graft pyelonephritis (AGPN).

Asymptomatic bacteriuria (ABU) is defined as in an asymptomatic patient in a clean-catch voided urine specimen with > 105 CFU/mL in two urine samples > 24 h apart or ≥102 CFU in a single catheterized urine specimen.

UTIs were also classified as a new infection, relapse, or re-infection.

Relapse was defined as the isolation of the same microorganism that caused the preceding infection in a urine culture obtained ≥2 weeks after finishing the previous treatment.

Re-infection was defined by a new episode of UTI with the isolation of an agent other than the one that caused the previous infection.

The diagnosis of urosepsis was made when simultaneous positive blood and urine cultures were obtained with the isolation of the same bacterial strain.

Statistical methods

The statistical analysis was carried out using Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, USA and version 23.0 for Windows). For normally distributed data, means were compared using Mann–Whitney U test for two groups. Kruskal–Wallis test was used for more than two groups. Categorical variables were demonstrated as frequencies and proportions. Proportions were compared using the Chi-square or Fisher's exact test, wherever applicable. All the risk factors were analyzed using multivariate analysis and assessed with Cox regression model, with forward selection technique. P < 0.05 was considered statistically significant.

  Results Top

Out of 300 renal transplant recipients, 107 (35.6%) patients suffered from UTI during the first 3-month postrenal transplant. Sixty-five patients received ABO-incompatible transplants. Three patients had undergone a deceased kidney donor transplant. The mean age in the UTI group was 32 years (standard deviation ± 10.5). No correlation between patients' age with the incidence of UTI development was observed. A slight female preponderance was observed. UTI was found in 64 (33.4%) of 192 male patients, whereas 43 (39.8%) of 108 female patients suffered from UTI. The most common etiology for end-stage renal disease (ESRD) was diabetic kidney disease, and it accounted for 48.3% of all ESRD causes. Other causes were chronic glomerulonephritis (29.33%), cystic kidney disease (3.3%), chronic interstitial nephritis (14.7%), and reflux nephropathy (4.33%). In patients with reflux nephropathy, preoperative evaluation was performed to rule out bladder outlet obstruction or spastic bladder. Patients with neurogenic bladder (n = 6) were included in the reflux nephropathy group. One transplant was on ileal conduit and three patients of neurogenic bladder were on clean intermittent catheterization to evacuate bladder following transplantation. Nearly 61% of patients with reflux kidney disease suffered from UTI. Almost 64.5% of all diabetic patients had UTI. In all diabetic patients, evaluation of bladder dysfunction was done, based on history, and clinical evaluation urodynamic studies were performed. Nearly 70% of patients with UTI were found to be having cystopathy. The median for the dialytic period before transplantation was 40 months (range 2 months to 268 months). Most of the patients were asymptomatic (55%). Out of these asymptomatic patients, on follow-up, 20% of patients developed symptomatic UTI. None was associated with pyelonephritis.

Effect of immunosuppressive medications on urinary tract infection

In our study, 290 patients received induction therapy immediately before the renal transplant surgery, and ten patients were not given any induction therapy. As per recommendations, induction with both polyclonal and monoclonal antibodies was used in high-risk recipients. Antithymocyte agent was used as an induction agent in 250 patients, and 40 patients received basiliximab. Sixty-six and 70 patients received rituximab and plasmapheresis, respectively, in desensitization protocol. Nearly 22.7% of patients with rituximab and 25.7% with plasmapheresis had UTI. Out of the 300 patients, 288 patients were receiving steroids, tacrolimus, and MMF for maintenance immunosuppression. None of the specific immunosuppressive medication or combination showed a statistically significant association with UTI. It has been shown in previous studies that ATG increases the number of infections in comparison with no-induction recipients significantly.[4],[5] However, in our study, we found no association of higher chances of UTIs in patients exposed to induction agents. Multivariate analysis also did not show an increase of UTIs with ATG induction in our study.

Timing of urinary tract infection

The rate of UTI was highest (55%) in the immediate posttransplant period within 7 days, followed by 20% after that in the 1st-month post-transplant. The rate of incidence decreases to 10% and 15% in the consecutive 2nd and 3rd month post transplant. Out of 27 patients in which UTI was observed during the 2nd and 3rd months, 6 (22%) patients had a previous episode of UTI [Figure 1].
Figure 1: Temporal incidence of urinary tract infection

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No statistically significant association of other transplant-related factors such as dialysis vintage, history of UTI any time before transplant, ABO-incompatible transplant, history of prior renal transplantation, and live or deceased donor with UTI was found in our study.

In patients suffering from obstructive uropathy or any other surgical complication such as lymphocele, surgical reexploration, Foleys catheter, and stent were kept in situ for a longer time as advised by the transplant surgeon. Prolonged Foley's catheter and indwelling double-J stent were predominant risk factors predisposing to UTI. The incidence of UTI increased from 30% with Foley's catheterization removed within 7 days, posttransplant, to 75% when the Foley's catheter was removed after 15 days. On multivariate analysis in our study, diabetes (P = 0.01), prolonged urethral catheterization (P = 0.002), double-J stent kept in situ (P = 0.03), and reflux kidney disease before transplant (P < 0.02) were independently associated with UTI, as shown in [Table 1].
Table 1: Multivariate analysis of risk factors for urinary tract infection development in renal transplant recipients

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Microbiological profile of patients with urinary tract infection

Most cases of UTI were caused by Gram-negative bacteria (88.5%). Gram-positive bacteria were responsible for 4.5% of cases, and fungi caused 7% of all UTI episodes. Among Gram-negative bacteria, the most common organism was Escherichia coli (41%) followed by Klebsiella spp. (16%). Other Gram-negative organisms were Acinetobacter baumannii (9%), followed by Pseudomonas (10%) and Proteus 6 (%). Enterobacter (4%) and Staphylococcus spp. (2%) accounted for most cases of Gram-positive bacterial infections. Mixed bacterial infections were present in 10% of all the cases, and 22% of all fungal infections were associated with a concomitant bacterial infection. Candida albicans (7%) was the most common fungi responsible for the UTI, as depicted in [Figure 2].
Figure 2: Microbiological profile of the patients with urinary tract infection

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Antibiotic resistance of pathogens

Klebsiella spp. was found to be the most resistant organism in our study. It was responsible for 80% of multidrug-resistant UTI. Other multidrug-resistant organisms were Acinetobacter baumannii, followed by Pseudomonas and Proteus. The resistance rates of Pseudomonas aeruginosa to ciprofloxacin and ceftazidime were reported to be 66% and 38%, respectively. In our study, Enterococcus faecalis had been reported to reach a resistance rate of 87% against ampicillin and 22% against vancomycin. Noteworthy, Acinetobacter showed a high resistance rate to imipenem (85%) and aztreonam (77%) in our study. The antibiotics resistance and sensitivity pattern of these pathogens is shown in [Table 2] and [Figure 3], respectively. In multidrug-resistant UTI, culture sensitivity to other antibiotics such as fosfomycin was performed, which is not usually done in our microbiology laboratory and according to their reports, treatment was given. Most of these patients were treated with ceftazidime/avibactam combination, double carbapenem combination, and intravenous fosfomycin.
Table 2: Pathogens resistance to antibiotics (%)

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Figure 3: Antibiotic sensitivity pattern of microorganisms causing urinary tract infection

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  Discussion Top

The presence of UTIs among renal allograft recipients is variable in different studies. It ranges from 23% to 60%, and it accounts for approximately 44%–47% of all infections.[6] In our study, the prevalence of UTIs among renal allograft recipients was 35.6%. Out of 300 patients, 107 patients suffered from UTI. In most of the studies, UTIs were more common in the early posttransplant period, particularly in the 1st year (74%), after that incidence decreases to <35% at the 2nd year, and it further decreases to 20% at 5 years post transplant. This is probably due to the surgical trauma, placement of urinary catheter/ureteral stent, and the need for a higher level of immunosuppression.[7] In our study, most of the UTI episodes were present in the first 7 days posttransplant (55%), and its frequency decreased subsequently to 10% and 15% percent in the 2nd and 3rd months, respectively.

Our study demonstrated a slightly higher predisposition of UTI in females than males. This finding was supported by a retrospective study on kidney transplant recipients, which found that the cumulative rate of UTI on follow-up of 4 years was 60% for females.[3] This can be explained by the difference in anatomical features of the urinary tract of females, such as the short urethra, but other authors did not confirm this finding.[4]

Various studies have shown conflicting results concerning the association of the recipient's age and UTI. As observed in other studies [5],[6] in our study also, no relation could be established between recipients' age with UTI. Benign prostatic hypertrophy and bladder atrophy may be attributing factors to the increased risk of UTI in the elderly population. Our study showed no association of the increase in the risk of developing UTI in recipients of deceased kidney donors, which has been observed by Glazier et al.[8],[9] Prolonged ischemia time, delayed recovery of graft function, or possibly from the use of more intense immunosuppression leads to a higher risk of UTI in recipients of cadaveric kidneys. Innumerable studies are demonstrating that urethral catheters increase the risk of UTI in both immunosuppressed and nonimmunosuppressed patients. Despite these reports, early removal of Foley catheters is not routinely followed. Our study reported the incidence of UTI at 27% when the urethral catheter was removed within 7 days, and it increased to 75% when the urethral catheter was removed after 15 days postoperatively.

The majority of the patients (55%) in our study included had ABU. Goh et al. reported a prevalence of ABU of 24% 1-month post transplant. Recently, in a survey by Fiorante et al., as many as 85% of were diagnosed as ABU cases in 3 years.[10] A high incidence of ABU was probably because of close surveillance done in our study. Urine culture was performed during each follow-up visit. As there are no recommendations for screening and treatment of ABU in renal transplant recipients, we did not treat cases of ABU in our study. As treatment of acute rejections (ARs) leads to increment in net immunosuppression, many authors mentioned that patients with AR are at a higher risk of UTIs and urosepsis [6] However, some other reports suggest that UTI can also trigger AR.[11] In our study, the time sequence between AR and UTIs was not analyzed.

Immunosuppressive medications are responsible for the suppression of the humoral and cellular immunity, predisposing transplant recipients to infections. Our study did not find any relationship of UTI with any particular medication or combination of maintenance immunosuppression. In contrary to this, Khanna et al. showed a significant association of UTI with the combination of cyclosporine, prednisolone, and azathioprine. They also reported that induction with basiliximab was associated with more UTI.[12]

CMV infection is related to an increase in net immunosuppression, and it predisposes to other infections by decreasing host immune response. In our study, only two patients suffered from CMV infection and none of them had UTI.

Pyelonephritis was not detected in any patient of UTI. In contrary to our study, Kamath et al. reported most episodes of AGPN within the first 3 months after renal transplant.[13]

The influence of double-J catheter use on the risk of UTI remains controversial. In our unit, double-J catheter was placed in all the patients of renal transplant to prevent major urological complications. Some reports showed that it is one of the important factors for the development of UTI after renal transplantation.[14] Others could not prove such a relationship.[15] Our study showed that the incidence of UTI increased with the number of days the double-J stent was kept in situ. A Cochrane systemic review compared early versus late ureteric stent removal after renal transplantation. The incidence of UTI was reduced in the early stent removal group designated as ureteric stent removal before the 3rd postoperative week.[16] The result of another meta-analysis by Yahav et al. did not demonstrate any significant difference in UTI rates between stent duration of <14 days or > 14 days. Certainly, additional randomized controlled trials are required to conclude that early removal of ureteral stents after renal transplant may be associated with reduced rates of UTI.

As with the general population, it was noticed that structural abnormalities increased the threat to developing UTIs in renal transplant recipients. Our study also showed a high risk of UTI incidence in patients with urinary malformation. Obstructive uropathy due to surgical complications, vesicoureteral reflux, neurogenic bladder, or prostate hypertrophy manifests as urine stasis with consequent graft ureteral and pelvis enlargement, representing a potential risk factor for the development of UTI. This is consistent with the results of Chuang et al. and Sqalli et al., who reported a higher UTI in patients with structural abnormalities.[17]

Diabetic nephropathy has been widely reported to be associated with an increased risk of UTI. This observation was also noticed in our study. Diabetes was the most cause of ESRD in our study. It accounted for 47% of cases. Out of 145 patients, 69 patients had UTI. This could be due to the significant number of diabetic patients in our study group. The incidence of UTI was higher in diabetic patients having cystopathy. Other causes of ESRD were not found to be a considerable cause for increasing UTI in our renal transplant recipients.

A similar study was done by Mukherjee et al., including 210 transplant recipients, in which 32.86% had UTI, with males (61.54%) predominantly affected in higher (>30 years) age group. E. coli was found to be the most common organism. Klebsiella pneumonia was frequently associated with multidrug resistance. Statistically significant predisposing factors for UTI were female sex, urinary tract alteration, prolonged urethral catheterization (P < 0.01), new-onset diabetes after transplantation, and coexisting hepatitis C infection.[18]

The strengths of our study were that it was a prospective observational study in which multiple independent identified risk factors predisposing to UTI were analyzed through multivariate analysis. Antibiotic resistance of pathogen was reported that can guide antibiotic treatment for a specific pathogen. Our study identifies multiple risk factors and can help to formulate strategies focused on particular risk factors. Our study was not without any shortcomings; important ones were a relatively smaller sample size. It was a single-center study, so generalization of the results may be limited. The proportion of patients with diabetic nephropathy as primary kidney disease was also relatively high. Even though multiple independent variables were identified as risk factors, some potential confounding factors and interactions among the factors were not evaluated. As the study period was until the initial 3 months posttransplant, the long-term effect of UTI on graft outcome could not be scrutinized.

  Conclusion Top

In our study, multivariate analysis revealed that diabetes mellitus, number of days of ureteral catheterization, and Double-J stent kept in situ and reflux nephropathy were independently associated with the development of UTI.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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Gondos 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.  Back to cited text no. 2
Espinar 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.  Back to cited text no. 3
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Glazier DB, Jacobs MG, Lyman NW, Whang MI, Manor E, Mulgaonkar SP. Urinary tract infection associated with ureteral stents in renal transplantation. Can J Urol 1998;5:462-6.  Back to cited text no. 8
Martinez-Marcos F, Cisneros J, Gentil M, Algarra G, Pereira P, Aznar J, et al. Prospective study of renal transplant infections in 50 consecutive patients. Eur J Clin Microbiol Infect Dis 1994;13:1023-8.  Back to cited text no. 9
Fiorante S, López-Medrano F, Lizasoain M, Lalueza A, Juan RS, Andrés A, et al. Systematic screening and treatment of asymptomatic bacteriuria in renal transplant recipients. Kidney Int 2010;78:774-81.  Back to cited text no. 10
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Mathe Z, Treckmann JW, Heuer M, Zeiger A, Sauerland S, Witzke O, et al. Stented ureterovesical anastomosis in renal transplantation: Does it influence the rate of urinary tract infections? Eur J Med Res 2010;15:297-302.  Back to cited text no. 14
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