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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 30  |  Issue : 5  |  Page : 211-215

Characteristics of bacterial colonization after indwelling ureteral stents in urinary stone patients with diabetes mellitus and chronic kidney disease


1 Department of Urology, Medical Faculty of Udayana University/Sanglah General Hospital, Denpasar, Bali, Indonesia
2 Department of General Surgery, Medical Faculty of Udayana University/Sanglah General Hospital, Denpasar, Bali, Indonesia
3 Department of Neurosurgery, Medical Faculty of Udayana University/Sanglah General Hospital, Denpasar, Bali, Indonesia

Date of Submission10-Oct-2018
Date of Decision19-Nov-2018
Date of Acceptance21-Dec-2018
Date of Web Publication24-Oct-2019

Correspondence Address:
Gede Wirya Kusuma Duarsa
Department of Urology, Sanglah General Hospital, Jl. Kesehatan No. 1, Denpasar, Bali 80114
Indonesia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/UROS.UROS_124_18

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  Abstract 


Background: Placement of ureteral stents has been standard after the endoscopic procedures because it relieves obstruction caused by the stone and facilitates urine drainage. Bacterial colonization in the stent plays an essential role in the pathogenesis of stent-associated infections. The goal of this study was to determine the frequency, type of pathogens, and the significance of risk factors that may affect bacterial colonization of ureteral stents after endourology procedures in urinary stone patients. Methods: Thirty patients underwent percutaneous nephrolithotomy or ureterorenoscopy for renal and ureteric stones were enrolled in this study. Urine specimens were collected for culture examination before stent insertion and on removal. The stents were then removed based on the clinical decision via the cystoscope, and three distal tip segments of the stents were sent for culture examination. Results: Four patients (13.3%) before stent insertion and 11 patients (36.7%) before stent removal had positive urine cultures. Eighteen (60%) stents were positive for the culture. Diabetes mellitus (DM) (P = 0.018) and chronic kidney disease (CKD) (P = 0.040) had a significant difference in increasing the risk of bacterial colonization. Pseudomonas aeruginosa was the most common pathogen isolated from the stent culture. Conclusion: An indwelling ureteral stent carries a significant risk of bacterial colonization both on patients with DM and also CKD. P. aeruginosa appears as the most common bacteria in stent culture due to immunocompromised factors of these patients.

Keywords: Bacteriuria, colonization, DJ stent, urinary stone


How to cite this article:
Gede Oka AA, Kusuma Duarsa GW, Wulandari SR, Bagus Mahadewa TG, Santosa B, Yudiana W, Tirtayasa PW. Characteristics of bacterial colonization after indwelling ureteral stents in urinary stone patients with diabetes mellitus and chronic kidney disease. Urol Sci 2019;30:211-5

How to cite this URL:
Gede Oka AA, Kusuma Duarsa GW, Wulandari SR, Bagus Mahadewa TG, Santosa B, Yudiana W, Tirtayasa PW. Characteristics of bacterial colonization after indwelling ureteral stents in urinary stone patients with diabetes mellitus and chronic kidney disease. Urol Sci [serial online] 2019 [cited 2019 Nov 22];30:211-5. Available from: http://www.e-urol-sci.com/text.asp?2019/30/5/211/269883




  Introduction Top


Endoscopic surgery has been the choice of treatment for patients with renal and ureteric stones. Placement of ureteral stents has been standard after the endoscopic procedures because it relieves obstruction caused by the stone and facilitates urine drainage.[1]

Stents are synthetic biomaterials with suitable surfaces for bacterial colonization, because of the development of biofilm around these stents.[2] Stents are considered to develop infectious complications, where 80% of postprocedural infections in urology are secondary to indwelling stents.[1] Such urinary tract infections (UTIs) account for >40% of nosocomial infections and are mostly caused by a planktonic form of single bacterium amenable to treatment with susceptible drugs.[3]

Bacterial colonization in the stent plays an essential role in the pathogenesis of stent-associated infections. It normally remains clinically silent, but the colonized stents may be the origin of complicated UTI and can lead to sepsis.[4] Systemic antibiotic therapy is effective in eliminating planktonic or circulating bacteria, but it usually fails to protect the surface of materials from colonization.[5] Risk factors are bound to the patient and can affect the appearance of bacteria due to the presence of foreign bodies in the urinary tract. Sometimes, it is difficult to distinguish bacteriuria caused by urological instrumentation from urine contamination with periurethral flora.[6]

Most UTIs originate from the patient's colon flora.[7] In the infection associated with urological instrumentation, most uropathogens can form complex biofilm groups including Gram-positive and Gram-negative bacteria, as well as fungi.[8],[9] The goal of this study was to determine the frequency, type of pathogens, and the significance of risk factors that may affect bacterial colonization of ureteral stents after endourology procedures in urinary stone patients.


  Methods Top


This was a prospective study with consecutive sampling. Thirty patients with renal and/or ureteric stones underwent percutaneous nephrolithotomy and ureterorenoscopy with stent placement were enrolled in this study. All patients included in this study did not have a previous UTI history, which was known from the absence of complaints leading to UTI. Positive urine culture which obtained prior to procedure, indicated the presence of asymptomatic bacteriuria and we still included in this study to analyzed the consistent of emergences of infection in the next urine and stent culture examination after the endourological procedure was taken. This study had been approved by the Committee of Ethical Research of our university. All involved patients have provided written consent to be included in this study.

All patients were given intravenous prophylactic antibiotic with 2 g of cefazolin. Ten-milliliter midstream urine from all the patients was investigated microbiologically before stent insertion and, on the day of stent removal, inoculated into blood agar and MacConkey agar. Plates were kept in 37°C for 24 h. Positive urine or “significant bacteriuria” culture was defined as ≥105 colony-forming units/ml of urine with the culture yielding only one or two bacteria/fungi. More than two species of bacteria in urine samples were categorized as pathogenic. Stents were then removed within 15–60 days through the cystoscope. Three of the distal segments of the stent were sent for culture. Stent colonization was defined as a colony count of ≥10 per plate. Data such as age, sex, duration of stenting, the presence of diabetes mellitus (DM), obesity (Body mass index over 30 kg/m2), and chronic kidney disease (CKD) were recorded.

Analyses were performed using SPSS version 23 for Windows (IBM, Armonk, NY, United States of America). We used Chi-square and Fisher's exact tests and logistic regression for multivariate analysis. The results were considered statistically significant when P < 0.05.


  Results Top


Thirty patients consisted of 23 males and 7 females (23.3%) in the age range of 18–65 years. The average stent indwelling time was 37.1 days. Bacteriuria before stenting was found in 4 (13.3%) patients, and 11 (36.7%) patients had bacteriuria after stent insertion. From microbiological culture examination of the stents after stent removal, bacterial colonization was found in 18 (60%) patients. Characteristics of the patients are shown in [Table 1].
Table 1: Patients' characteristics (n=30)

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[Table 2] shows that from the 7 (23, 3%) female patients, 5 (71, 4%) yielded colonized stents, whereas 13 (56, 5%) of the 23 (76, 7%) male patients had colonization of their stents, so the ratio infection was more common in female than male (0,7:0,6), but this difference is not statistically significant. Stents removed within 30 days of insertion had a lower rate of positive stent culture compared to stents removed after 30 days (6 vs. 12). Out of 8 patients with a history of diabetes, 7 (87.5%) were found developed bacterial colonization.
Table 2: Bivariate analysis for each variables to bacterial colonization of the ureteral stent

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We analyzed the multivariate analysis with logistic regression for these variables [Table 3] and found that bacterial colonization was not associated with patient's age (P = 0.213), sex (P = 0.805), and the duration of stenting (P = 0.195). On the other hand, both diabetes (P = 0.018) and CKD (P = 0.040) had a significant difference in relation to bacterial colonization.
Table 3: Multivariate analysis for each variables to bacterial colonization of the ureteral stent

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The types of microorganism in urine culture before and after stenting and stent culture are shown in [Table 4]. We found the emergences of 2 type of microorganism in 1 sample of urine culture in the day of stent removal. We used the McNemar's test [Table 5] and [Table 6] to see if it has any significant value. P value was 0.039 between both urine cultures and 0.016 between urine culture after stenting and stent culture. Patients with bacteriuria at the beginning of a urine culture examination consistently continued to appear on postoperative urine culture examination, which also mean that bacteriuria before stenting had significant risk to bacteriuria after stenting (P<0,05). Similarly, bacteriuria after stenting had significant risk to bacterial colonization (P<0,05).
Table 4: Bacteriology results of urine and stent culture

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Table 5: Bacteriological analysis between urine culture before stenting and before stent removal

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Table 6: Bacteriological analysis between urine culture before stent removal and the results of stent culture

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  Discussion Top


Urine culture is not particularly a sensitive mean of detecting stent colonization; therefore, a negative culture does not rule out a colonized stent. We found bacterial colonization in 60% of ureteral stents and 36.7% of bacteriuria after stenting.

Another report mentioned that sex difference was not significant,[10] which is similar to our study. The greater number of male patients in this study, the incidence of urinary tract stones is more prevalent in males.[11] The increase in bacterial colonization in stents derived from patients older than 50 years,[2] but we found the rate of bacterial colonization in each age category had same proportion and the results were not statistically significant as in previous study.[10]

Although the colonization rates were higher for those with stents inserted for category 31–60 days, the difference was not statistically significantly similar to Aydin's study.[10] However, when it is considered that the stents will remain in the majority of patients for around 30 days, the longer duration will likely increase the risk of colonization. Obesity has been known related to metabolic syndromes, such as DM and both correlated with systemic inflammation. It was stated that obesity may stimulate the increase of pro-inflammatory substances.[12] In our study, patients with obesity had 1.1 higher risk for colonization rate but statistically not significant (P = 0.107). It can be assumed that obese patients in this study did not suffer from DM as a result of complications from obesity.

In this study, DM and CKD was significantly affected bacterial colonization of ureteral stent (P< 0.05). These results are supported by the previous study.[13] Type 2 DM and CKD are two diseases that can decrease the immune system, leading to high risk for bacterial colonization of ureteral stent, because they affect the immune system by decreasing the natural extrinsic and intrinsic defense mechanisms of the bladder, thereby increasing the occurrence of bacteriuria similar to colonization of ureteral stent bacteria.[14]

Ureteral stent placement or catheterization often promotes ascending infections by the commensals present in the urethra. In bladder environment, some organisms can multiply rapidly if urine is not drained continuously.[3] Human macrophages more efficiently phagocytized planktonic bacteria than biofilm bacteria.[15] The difference between how each interacts with macrophages could be due to their dissimilar external structures: whereas planktonic bacteria are individual microorganisms, the biofilm is a well-connected organization of millions of them. The first stage of a pathogenic infection is typically caused by planktonic bacteria that are detached from a mature biofilm. Bacterial adherence is crucial to both colonize the niche and develop a new biofilm structure, which usually represents a challenge to the immune system and bacterial adhesion appeared to depend on the virulence-associated characteristics of the bacteria.[15]

 Escherichia More Details coli is the most common bacteria found in bacteriuria and stent culture,[9],[10] but in our study, microorganism that identified from the stent culture was similar with urine culture after stenting and we found that the most common bacteria is Pseudomonas aeruginosa followed by E. coli. Similar with our study, Chatterje et al. also found P. aeruginosa as the most common bacteria in stent colonization.[3]P. aeruginosa is a Gram-negative, aerobic bacterium that is ubiquitous in the environment and it is an opportunistic pathogen, rarely infecting healthy individuals, but can cause chronic biofilm infections in immunocompromised individuals.[16] These data support our results that stent colonization is more commonly present in patients with DM and CKD and the type of bacteria that make up colonization caused by decreased of immune systems, but its presence in urine as circulating bacteria can still be eliminated by prophylactic antibiotics, as seen in our results where the number of positive stent cultures was greater than positive urine cultures after stenting.


  Conclusion Top


Because only a small percentage of urinary cultures identified all colonizing microorganisms correctly and as there was a great discrepancy between urine and stent cultures, removal and bacteriologic evaluation of ureteral stents may be necessary in the case of infection. An indwelling ureteral stent carries a significant risk of stent colonization, and the significant correlation was noted between DM and CKD. P. aeruginosa appears as the most common bacteria in stent culture due to immunocompromised factors of these patients. The use of prophylactic antibiotics seems effective to eliminate potential intruders of the urinary tract before their adhesion to the stents, but it will not prevent the attachment and biofilm formation of microorganisms that are already resistant.

Ethical clearance information

IRC Institution Name: Commission of Ethical Research, Faculty of Medicine, Udayana University/Sanglah General Hospital, Denpasar, Bali, Indonesia Ethical Clearance No: 2589/UN.14.2/KEP/2017, Approval Date: December 8th, 2017.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Javed MS, Subhani GM, Tahir S, Javed SH. Significance of indwelling time for bacterial colonization of double J stents. APMC 2016;10:36-40.  Back to cited text no. 1
    
2.
Bonkat G, Rieken M, Rentsch CA, Wyler S, Feike A, Schäfer J, et al. Improved detection of microbial ureteral stent colonisation by sonication. World J Urol 2011;29:133-8.  Back to cited text no. 2
    
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Chatterjee S, Maiti P, Dey R, Kundu A, Dey R. Biofilms on indwelling urologic devices: Microbes and antimicrobial management prospect. Ann Med Health Sci Res 2014;4:100-4.  Back to cited text no. 3
[PUBMED]  [Full text]  
4.
Elwood CN, Lo J, Chou E, Crowe A, Arsovska O, Adomat H, et al. Understanding urinary conditioning film components on ureteral stents: Profiling protein components and evaluating their role in bacterial colonization. Biofouling 2013;29:1115-22.  Back to cited text no. 4
    
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Grabe M, Botto H, Cek M, Tenke P, Wagenlehner FM, Naber KG, et al. Preoperative assessment of the patient and risk factors for infectious complications and tentative classification of surgical field contamination of urological procedures. World J Urol 2012;30:39-50.  Back to cited text no. 7
    
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Lo J, Lange D, Chew BH. Ureteral stents and foley catheters-associated urinary tract infections: The role of coatings and materials in infection prevention. Antibiotics (Basel) 2014;3:87-97.  Back to cited text no. 8
    
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Kliś R, Szymkowiak S, Madej A, Blewniewski M, Krześlak A, Forma E, et al. Rate of positive urine culture and double-J catheters colonization on the basis of microorganism DNA analysis. Cent European J Urol 2014;67:81-5.  Back to cited text no. 9
    
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Aydin HR, Irkilata L, Aydin M, Gorgun S, Demirel HC, Adanur S, et al. Incidence of bacterial colonisation after indwelling of double-J ureteral stent. Arch Ital Urol Androl 2016;87:291-4.  Back to cited text no. 10
    
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Pearle MS, Lotan Y. Urinary lithiasis: Etiology, epidemiology, and pathogenesis. In: Campbell-Walsh Urology. 10th ed. USA: Elsevier-Saunders; 2012. p. 1257-86.  Back to cited text no. 11
    
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Hainer V, Zamrazilová H, Kunešová M, Bendlová B, Aldhoon-Hainerová I. Obesity and infection: Reciprocal causality. Physiol Res 2015;64 Suppl 2:S105-19.  Back to cited text no. 12
    
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Al-Ghazo MA, Ghalayini IF, Matani YS, El-Radaideh KM, Haddad HI. The risk of bacteriuria and ureteric stent colonization in immune-compromised patients with double J stent insertion. Int Urol Nephrol 2010;42:343-7.  Back to cited text no. 13
    
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Altunal N, Willke A, Hamzaoǧlu O. Ureteral stent infections: A prospective study. Braz J Infect Dis 2017;21:361-4.  Back to cited text no. 14
    
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Hernández-Jiménez E, Del Campo R, Toledano V, Vallejo-Cremades MT, Muñoz A, Largo C, et al. Biofilm vs. planktonic bacterial mode of growth: Which do human macrophages prefer? Biochem Biophys Res Commun 2013;441:947-52.  Back to cited text no. 15
    
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Mikkelsen H, Duck Z, Lilley KS, Welch M. Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J Bacteriol 2007;189:2411-6.  Back to cited text no. 16
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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