Characteristics of Double-J Stent Encrustations and Factors Associated with their Development Jian Huang1,2*, Weizhou Wu1*, Shike Zhang1*, Yapeng Huang1, Tao Zeng1, Lingyue An1, Yeping Liang1, Jinkun Huang1, Hans-Göran Tiselius3, Guohua Zeng1#, Wenqi Wu1,4# Purpose: To evaluate the chemical composition of double-J stent encrustation and to assess risk factors associated with their development. Materials and Methods: Patients who had double-J stents removed between July 2016 and June 2017 were recruited for this study prospectively. The clinical features of the patients were recorded and the composition of encrustation material was analyzed by infrared spectroscopy. Results: Encrustments from a total of 372 double-J stents were collected. The mean age of patients was 50.4±13.1 years and deposits possible to analyze were obtained from 228 males (61.3%) and 144 females (38.7%). Calcium oxalate monohydrate was the most common constituent of stone and encrustments. The encrustation rate of vesical coils was significantly higher than that of renal coils (P < 0.001). There was no significant difference in chemical composition between stone and encrustation regarding renal (P = 0.086) and vesical coils (P = 0.072). The only predictive risk factor for the development of encrustation on double-J stents was indwelling time. This phenome- non was observed in both renal (P < 0.001) and vesical coils (P = 0.021). Interestingly, patient with chronic kidney disease (CKD) was associated with less risk of encrustation on both renal (P < 0.001) and vesical coils (P = 0.001). Conclusion: The chemical composition of double-J stent encrustation was the same as the urinary stone. The prevention strategy for stone composition is also suitable for the prevention of encrustation of double-J stent. The only predictive factor for double-J stent encrustation was the indwelling time. CKD patient was shown to be less at risk for the development of encrustation. Keywords: Double-J stent; encrustation; chemical composition; urolithiasis; renal coil; vesical coil INTRODUCTION In 1967, Zimskind et al. were the first to use silicone ureteral splints to remedy ureteral obstruction(1). In 1978, Finney introduced a neoteric double-J stent with a hook molded into each end with the purpose of add- ing a self-retaining function and preventing migration(2). With this innovation, double-J stent became a funda- mental device in many urological procedures such as the management of patients with obstructing ureteral stone, ureteral or ureteropelvic junction strictures, ret- roperitoneal tumors or fibrosis. Also, stent is regular af- ter laparoscopic or open urologic surgery(1,3). The dou- ble-J stent serves as a significant therapeutic option to moderate the obstruction and counteract renal failure (4). However, there are several side effect accompanied by the insertion of double-J stent, such as flank pain, stor- age symptoms, dysuria and hematuria, etc.(5). Moreover, as a foreign body within the collecting system, there is 1Department of Urology, Minimally Invasive Surgery Center, The First Affiliated Hospital of Guangzhou Medical University, Guangdong Key Laboratory of Urology, Guangzhou Institute of Urology, Guangzhou, China. 2Laboratory of Urology, Affiliated Hospital of Guangdong Medical University, Zhanjiang, Guangdong, China. 3Division of urology, Department of Science, Intervention and Technology, Karolinska Institute, Stockholm, Sweden. 4Department of Urology, The Second Affiliated Hospital of Guangzhou Medical University. *Correspondence: 1Department of Urology, Minimally Invasive Surgery Center, The First Affiliated Hospital of Guangzhou Medical University, Guangdong Key Laboratory of Urology, Guangzhou Institute of Urology, Guangzhou, China. 2Department of Urology, The Second Affiliated Hospital of Guangzhou Medical University Tel: +86 13609089242. Fax: 0086-2034294141. E-mail: wwqwml@163.com. Received November 2020 & Accepted July 2021 concern that the double-J stent will be subject to deposi- tion of organic and mineral material, contributing to the formation of stone and encrustation(6-7). Accordingly, it was assumed that encrustation on stents was caused by deposition of layers of organic material, uropathogens and salt in urine(8). It’s reported that the bacteria adher- ing to a double-J stent is the main process of biofilm formation. The aggregation of the biofilm produced by the bacteria and the precipitated urinary components causes the formation of double-J stents encrustation(9-12). Encrustation may occur on renal and vesical coils of double-J stent. Severe encrustation of the stent may pre- vent stent removal in the traditional, routine transure- thral manner. The removal of encrusted stents, thus, is a challenging problem of clinical urology(13). Focusing on methods aiming at prevention of encrustation is im- portant. There is, however, a shortage of information on the characteristic of stent encrustation, such as their risk ENDOUROLOGY AND STONE DISEASE Urology Journal/Vol 19 No. 1/ January-February 2022/ pp. 22-27. [DOI: 10.22037/uj.v18i.6578] Vol 19 No 1 January-February 2022 138 Risk factors of double-J stent encrustations-Huang et al. Renal coil Vesical coil Index Value Encrustation (%) No encrustation (%) p value OR Encrustation (%) No encrustation (%) p value OR Total, n (%) 372 (100) 239 (64.2) 133 (35.8) 277 (74.5) 95 (25.5) Age, years 50.4±13.1 50.4±13.3 50.1±12.8 0.855 - 50.3±13.0 50.4±13.6 0.969 - Gender, n (%) 0.439 0.841 0.498 0.846 Male 228 (61.3) 143 (62.7) 85 (37.3) 167 (73.2) 61 (26.8) Female 144 (38.7) 96 (66.7) 48 (33.3) 110 (76.4) 34 (23.6) BMI, kg/m2 23.6±3.7 23.6±3.7 23.6±3.7 0.929 - 23.6±3.7 23.6±3.5 0.831 - Frequent stone 177 (47.6) 117 (66.1) 60 (33.9) 0.477 0.857 138 (78) 39 (22) 0.140 0.701 former, n (%) Hydronephrosis, 270 (72.6) 175 (68.4) 95 (35.2) 0.710 1.094 207 (76.6) 63 (23.3) 0.113 1.502 n (%) Chronic renal 67 (18.0) 30 (44.8) 37 (55.2) < 0.001 0.372 39 (58.2) 28 (41.8) 0.001 0.392 insufficiency, n (%) Preoperative urinary 145 (39.0) 91 (62.8) 54 (37.2) 0.632 0.900 108 (74.5) 37 (25.5) 0.994 1.002 tract infection, n (%) Stone location, n (%) Ureter 84 (22.6) 55 (65.3) 29 (34.5) 0.789 1.072 68 (81.0) 16 (19.0) 0.121 1.606 Kidney 228 (61.3) 151 (66.2) 77 (33.8) 0.316 1.248 164 (71.9) 64 (28.1) 0.159 0.703 Kidney and ureter 60 (16.1) 33 (55.0) 27 (45.0) 0.103 0.629 45 (75.0) 15 (25.0) 0.917 1.034 Stone free status, 232 (62.4) 149 (64.2) 83 (35.8) 0.990 0.997 175 (75.4) 57 (24.6) 0.581 1.144 n (%) Ureteral and/or 60 (16.1) 43 (71.7) 17 (28.3) 0.190 1.497 51 (85.0) 9 (15.0) 0.041 2.156 ureteropelvic junction stricture, n Double-J stent caliber, n (%) 0.213 1.313 0.210 1.350 5 Fr 152 (40.9) 92 (60.5) 60 (39.5) 108 (71.1) 44 (28.9) 6 Fr 220 (59.1) 147 (66.8) 73 (33.2) 169 (76.8) 51 (23.2) Indwelling time, n (%) < 0.001 - 0.019 - ≤ 14 days (9.5±3.5)d 48 (12.9) 17 (35.4) 31 (64.6) 28 (58.3) 20 (41.7) >14 days-1 month 133 (35.8) 85 (63.9) 48 (36.1) 99 (74.4) 34 (25.6) (24.1±4.7)d > 1 month-2 months 170 (45.7) 121 (71.2) 49 (28.8) 131 (77.1) 39 (22.9) (39.4±7.6)d > 2 months 21 (5.6) 16 (76.2) 5 (23.8) 19 (90.5) 2 (9.5) (108.9±70.6)d Stone composition, n (%) Calcium oxalate 163 (58.8) 103 (63.2) 60 (36.8) 0.657 0.893 120 (73.6) 43 (26.4) 0.637 1.137 monohydrate Calcium oxalate 21 (7.6) 14 (66.7) 7 (33.3) 0.811 1.122 16 (76.2) 5 (23.8) 0.698 1.228 dihydrate Ammonium 8 (2.9) 5 (62.5) 3 (37.5) 1 0.925 4 (50) 4 (50) 0.294 0.365 magnesium 40 (14.4) 28 (70.0) 12 (30.0) 0.413 1.353 31 (77.5) 9 (22.5) 0.449 1.358 phosphate Uric acid Carbonate apatite 43 (15.5) 26 (60.5) 17 (28.3) 0.572 0.825 28 (65.1) 15 (34.9) 0.234 0.658 Table 1. General characteristics of patients with stent encrustations Figure 1. Distribution of stone and renal coil encrustation com- position. p = 0.086 as analyzed with Bowker’s test of symmetry. Figure 2. Distribution of stone and vesical coil encrustation com- position. p=0.072 as analyzed with Bowker’s test of symmetry. Vol 19 No 1 January-February 2022 23 Endourology and Stones diseases 24 factors or chemical composition. For that reason, we prospectively collected data of patients with double-J stents in order to explore the features of stent encrusta- tion by separately considering renal and vesical coils. The aim was to evaluate the chemical composition of double-J stent encrustation and identify risk factors in- volved in the encrustation process. PATIENTS AND METHODS This study was approved by the Ethics Review Board of the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China. Informed consent was obtained from all individual patients included in the study. All double-J stents were obtained from patients who had been subject to stent removal at the First Affil- iated Hospital of Guangzhou Medical University. From July 2016 to June 2017, a total of 372 patients with the removal of double-J stents that had been part of their clinical treatment were recruited prospectively. All of the double-J stents were made of a material with a variety of medical applications, polyurethane, the most common polymeric biomaterial used in modern double-J stents(14). The baseline characteristics includ- ed age, gender, body mass index (BMI), frequent stone former, presence or absence of hydronephrosis, chronic kidney disease (CKD), preoperative urinary tract infec- tion, stone location, stone free status, ureteral and/or ureteropelvic junction strictures, double-J stent caliber, indwelling time, stone and the encrustation composi- tion. The variables were analyzed in a logistic regres- sion model, with the aim to find factors associated with the development of encrustation. To further elucidate the importance of the duration of stent treatment, the in- dwelling time was sub-grouped into four intervals: ≤ 14 days, >14 days to 1 month, >1 month to ≤ 2 months and >2 months. Generally, patients with indwelling time of double-J stent longer than 1 month were related to the ureteral stricture, ureteral injury or the delay of double-J stent removal with patients’ personal reason. Patients eligible for inclusion in the present study were those who were planned for removal of 5Fr or 6Fr dou- ble-J stents inserted because of urolithiasis and/or ure- teral/ureteropelvic junction strictures after nephroscope, ureteroscopy, laparoscope or open surgery. Computed Tomography (CT) scanning was used for the diagnosis of urinary stones. Ureteral and/or ureteropelvic junction strictures were diagnosed with intravenous pyelography (IVP), CT urography or ureteroscopy. The exclusion criteria were as follows: 1) a serious medical history of blood disease, family history of hereditary diseases, and other unusual conditions; 2) anatomical malformations including scoliosis, ectopic kidney, horseshoe kidney and polycystic kidney; 3) patients planned for urinary diversion or renal transplantation; 4) the stent was dis- placed. Moreover, only the data from the initial stent episode were included in case the same patient had been subject to repeated stent treatment. Patients with severe stone disease (frequent stone formers) were defined by frequent recurrence of stone after treatment or by stone surgery more than three times. The definition of CKD is described as the pres- ence of kidney damage (usually defined as urinary albumin excretion of ≥ 30 mg/day or equivalent) or decreased kidney function (detected as estimated glo- merular filtration rate (eGFR) < 60 mL/min/1.73m2) for three or more months, irrespective of the cause. Chronic kidney disease epidemiology collaboration (CKD-EPI) creatinine equation was used for the evaluation of the estimated glomerular filtration rate (eGFR)(15). All pa- tients were examined with plain film of kidney-ure- ter-bladder (KUB) and urinary ultrasound imaging before extraction of the stent. Patients were considered stone-free when no residual stones were detected in CT, KUB or urinary ultrasound examinations before extrac- tion of the double-J stents. Hydronephrosis was evalu- ated by a CT examination or ultrasonography, defined by dilatation of the renal pelvis or calices to a diameter exceeding 10mm according to the modification of the Grignon Grade system(16). Preoperative urinary tract infection was defined as a mid-stream sample of urine indicating bacterial growth ≥ 105 cfu/mL, or with a high level of leukocytes (sensitivity threshold: 104 leuko- cytes/mm3) or nitrites in the urine test strips, or with a positive urinary culture(17-18). Presence of encrustation Vesical coil Total Renal coil Encrustation No encrustation Encrustation 221 18 239 No encrustation 56 77 133 Total 277 95 372 Table 2. McNemar test for double-J stent encrustation of renal and vesical coils. Index Kidney Univariate Multivariable OR 95% CI P value OR 95% CI P value Age 1.002 0.985-1.018 0.854 Gender 0.841 0.543-1.304 0.439 BMI 1.003 0.946-1.062 0.929 Frequent stone former 0.857 0.560-1.311 0.477 Hydronephrosis 1.094 0.682-1.755 0.710 Chronic renal insufficiency 0.372 0.217-0.638 < 0.001 0.339 0.194-0.593 < 0.001 Preoperative urinary tract infection 0.900 0.583-1.388 0.632 Stone location 1.085 0.817-1.441 0.573 Stone free status 0.997 0.644-1.545 0.990 Ureteral and/or ureteropelvic junction stricture 1.497 0.816-2.746 0.192 Double-J stent caliber 1.313 0.855-2.018 0.214 Indwelling time ≤14 days < 0.001 < 0.001 >14 days to 1 month 3.229 1.621-6.433 0.001 3.366 1.669-6.788 0.001 >1 month to ≤2 months 4.503 2.285-8.873 < 0.001 5.006 2.499-10.026 < 0.001 >2 months 5.835 1.819-18.716 0.003 5.691 1.747-18.540 0.004 Stone composition 1.011 0.870-1.174 0.889 Table 3. Factors associated with the development of double-J stent encrustation of kidney. Risk factors of double-J stent encrustations-Huang et al. Vol 19 No 1 January-February 2022 138 was considered when visible chemical and mineralog- ical deposits covered the surface or lumen of the renal and vesical coils (approximately 6-8cm at each end of the stent). Their chemical composition was analyzed by infrared spectroscopy (Thermo Scientific Nicolet iS5). Under sterile conditions, the double-J stents were re- moved cystoscopically with an alligator forceps under local anesthesia. Stent fragments were dried by heating at 70ºC for 12 hours and then cooled at room tempera- ture. Subsequently, approximately 1mg of the dried en- crustation sample scraped from stent was evenly mixed with 200mg of potassium bromide, powdered, com- pressed into a small tablet, and finally scanned by Fou- rier transform infrared spectroscopy(19,20). According to the major chemical component that was recorded, the composition was classified as follows: calcium oxalate monohydrate, calcium oxalate dihydrate, ammonium magnesium phosphate, uric acid and carbonate apatite. In view of the rarity of cystine, ammonium urate, cal- cium phosphate, xanthine and 2,8-dihydroxyadenine, these constituents were referred to “other composition”. The composition of the stone was compared with the composition of encrustation at the renal and vesical coils of the stent. Statistical Analysis The SPSS software version 16.0 was used to perform the statistical analysis. The significance level was de- fined as p-values less than 0.05. Continuous variables were presented as means ± standard deviation (SD). Categorical variables were expressed as frequency and percentage. McNemar test was used for group compar- ison. Bowker’s test of symmetry was used to compare the composition of urinary stones and double-J stent en- crustation. Unconditional logistic regression was used and expressed as odds ratios (OR) and 95% confidence intervals (95% CI) to identify independent factors as- sociated with the formation of stent encrustation. Vari- ables with p-values less than 0.1 in univariate analysis were regarded as important factors, and they were fur- ther examined in the multivariable analysis. RESULTS A total of 372 double-J stents were collected prospec- tively and included in this study. Patients’ demograph- ics and the characteristics of patients with or without encrustation were listed in Table 1. The mean age of patients was 50.4 ± 13.1 years. There were 228 males (61.3%) and 144 females (38.7%) with a male to female ratio of 1.60:1. The most common stone constituent was calcium oxalate monohydrate (58.8%). There were 77 stents without any encrustation. A total of 277 stents were encrusted with vesical coil and 239 stents had encrustation in the renal coil. The encrusted rate of vesical coils (74.5%) was significantly higher than that in the renal coil (64.2%) when analyzed with the McNemar method (P < 0.001) (Table 2). Figure 1 and Figure 2 show the comparison between the composition of stone and encrustation. Only those patients with analysis of stone and encrustation simul- taneously were included. A comparison with Bowker’s test of symmetry didn’t demonstrate any significant difference about the chemical composition between stone and double-J stent encrustation in both of renal (178 patients, P = 0.086) and vesical (201 patients, P = 0.072) coils. This result means that the composition of double-J stent encrustation was more likely to be the same as that of the stone. A regression analysis model was established to analyze the potential variables that were related to the formation of double-J stent encrustation (Table 3 and Table 4). The parameters including age, gender, body mass index (BMI), frequent stone former, hydronephrosis, preoper- ative urinary tract infection, stone location, stone free status, ureteral and/or ureteropelvic junction stricture, double-J stent caliber and stone composition had no ef- fect on the formation of encrusted double-J stents when analyzed in the logistic regression model. The only pre- dictive risk factor for development of stent encrustation was the indwelling time for both renal (P < 0.001) and vesical (P = 0.021) coils. Interestingly, CKD patient was shown to be less risk for development of encrus- tation of renal (OR 0.339, 95% CI: 0.194-0.593, P < 0.001) and vesical (OR 0.383, 95% CI: 0.217-0.675, P = 0.001) coils. DISCUSSION Identification of the characteristics of double-J stent encrustation and search for related factors are of impor- tance for the prevention and treatment of encrustation. Observations in this study indicated that the vesical coil was more prone to encrustation than the renal coil. The Table 4. Factors associated with the development of double-J stent encrustation of bladder. Bladder Index Univariate Multivariable OR 95% CI p value OR 95% CI p value Age 1.000 0.982-1.018 0.969 Gender 0.846 0.522-1.372 0.499 BMI 1.007 0.945-1.073 0.831 Frequent stone former 0.701 0.438-1.124 0.141 Hydronephrosis 1.502 0.907-2.487 0.114 Chronic renal insufficiency 0.392 0.225-0.684 0.001 0.383 0.217-0.675 0.001 Preoperative urinary tract infection 1.002 0.621-1.615 0.994 Stone location 0.808 0.599-1.090 0.162 Stone free status 1.144 0.709-1.844 0.581 Ureteral and/or ureteropelvic 2.156 1.018-4.569 0.045 junction stricture Double-J stent caliber 1.350 0.844-2.160 0.211 Indwelling time ≤14 days 0.025 0.021 >14 days to 1 month 2.080 1.039-4.161 0.039 2.128 1.051-4.308 0.036 >1 month to ≤ 2 months 2.399 1.220-4.717 0.011 2.580 1.294-5.146 0.007 > 2 months 6.786 1.417-32.485 0.017 6.546 1.351-31.706 0.020 Stone composition 1.018 0.861-1.204 0.835 Risk factors of double-J stent encrustations-Huang et al. Vol 19 No 1 January-February 2022 25 only risk factor for the formation of encrustation was the time that stent had been indwelling in the collecting system. CKD was found to associate with less double-J stent encrustation. This series of measurements provide the first report on a reduced risk of stent encrustation in patients with CKD. In this study, the vesical coil was observed to have a higher rate of encrustation than the renal coil. The un- derlying cause is probably attributable to the storage function of urine in the bladder, with increased expo- sure time of the stent to urine. Furthermore, Sighinolfi et al. reported that urinary tract infection was related to encrustation of vesical coils(6). Lower urinary tract in- fection is more common than upper urinary tract infec- tion, which might provide another explanation for the fact that vesical coils have a higher rate of encrustation than renal coils. However, in our series, preoperative urinary tract infection did not affect the encrustation of double-J stent in the regression model. It was a short- coming that the current research lacks data of postoper- ative urinary tract infection, which might be more per- suasive to explain the connection between urinary tract infection and double-J stent encrustation. Rouprêt et al. recorded a 71.4% correlation between stent encrustation and stone composition and concluded that analysis of the chemical composition of encrusta- tion could be a possible method for conclusions on stone composition in the case of a stone has not been acquired for analysis(21). Similar findings were also described by Bariol and colleagues(22). In our series, the Bowker’s test of symmetry conducted to authenticate the chem- ical composition of double-J stent encrustations was more likely to be the same as that of the urinary stone, which means the prevention strategy for stone compo- sition is also useful for the prevention of encrustations of double-J stent. Rouprêt et al. indicated that there was no significant difference in the composition of encrusta- tion at the ends of the stent(21). Moreover, our series pre- sented that calcium oxalate monohydrate was found to be the most common stone or encrustation component. Calcium oxalate monohydrate is mainly associated with hyperoxaluric states(23). It can also come from the crys- talline conversion of calcium oxalate dihydrate, thus, be initiated by transient hypercalciuria(24,25). Venkatesan and colleagues blamed the encrustation of calcium oxa- late to a consequence of its poor solubility(26). After adjustment of all statistically significant variables from the univariate analysis, the multivariable logistic regression model indicated that indwelling time was the only predictive risk factor associated with encrust- ed double-J stents in both renal and vesical coils. The same phenomenon was also described by Sancaktutar and Eisenberg et al.(27,28). The rate of chemical and min- eralogical encrustation increases with the indwelling time. Sighinolfi et al. have mentioned that urolithiasis patients, especially in frequent stone formers, were re- lated to the burden of renal coil encrustation(6). How- ever, urinary tract infection and patient’s aging were the risk variables contributing to the higher degrees of vesical coil encrustation. This phenomenon was related to a bladder outlet dysfunction. In this series, patient with CKD was associated with less risk of double-J stent encrustation for both renal and vesical coils. There is reason to convince that CKD as a special physiological status being against the for- mation of kidney stones. Craver and colleagues con- ducted a cross-sectional study for the analysis of min- eral metabolism alterations in CKD(29). A total of 1836 patients were included and classified into stages 1-5. Results indicated that there is an associated fall in urine calcium excretion when GFR declines. It is well recog- nized that urine calcium is one of the most important critical risk factors for stone formation(23,30). Marangel- la et al. investigated in 171 patients with chronic renal insufficiency, presented that multiple changes in renal pathophysiology were connected to the onset of renal insufficiency, which result in a sharp decrease in the urine saturation with respect to calcium salts(31). These changes account for the decrease in the stone recurrence rate in the impaired GFR patients. Also, the reduction in urine calcium excretion in patients with CKD seems to contribute to the less double-J stent encrustation. There are several shortcomings inherent in the design of this study to which attention should be paid. Firstly, lack of data of postoperative urinary tract infection, bac- teriuria, medication therapy, daily water intake and diet, did not enable us to exactly elucidate the possible im- pact of infection, medication therapy, daily water intake and diet on encrustation. Secondly, stent characteristics were heterogeneous both in terms of brand and length. Finally, without the degree of quality of encrustation, hindering us to further understand the relationship of encrustation and indwelling time. CONCLUSIONS In this series, the chemical composition of double-J stent encrustation was more likely to be the same as that of the urinary stone, which means the prevention strategy for stone composition is also useful for the pre- vention of encrustation of double-J stent. The results showed that CKD patient had less risk on development of encrustation. Indwelling time was the only predictive risk factor for development of double-J stent encrusta- tion. The observations provides a basis for further con- siderations on the prevention and treatment of patients with double-J stent encrustation. ACKNOWLEDGEMENT This work was financed by National Natural Science Foundation of China (81570633) and The Science and Technology Project of Guangdong province, (2017B030314108) and Education Bureau Project of Guangdong province (2018KZDXM056). REFERENCES 1. Zimskind PD, Fetter TR, Wilkerson JL. Clinical use of long-term indwelling silicone rubber ureteral splints inserted cystoscopically. 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