KIDNEY TRANSPLANTATION Comparison of Removing Double-J Stent With and Without Cystoscopy in Kidney Transplant Patients: A Randomized Clinical Trial Mohammad Nadjafi-Semnani1*, Nasser Simforoosh1, Abbas Basiri1, Ali Tabibi1, Ali Nadjafi-Semnani2 Purpose: The ureteric stent can be attached to the Foley catheter in kidney transplantation to exclude cystoscopy for its removal. It is rarely practiced in renal transplantation. There has been no randomized trial to evaluate the outcome of this procedure on major urologic complications. Materials and Methods: One hundred sixty-three kidney transplant patients were randomized into an intervention group in which the stent was attached to the Foley catheter and removed together and a control group in which stent was removed by cystoscopy. In both groups, stents were removed around the 8th post-operative day. Results: From March 2016 to June 2017, out of 234 kidney transplants performed in our center, one hundred Sixty-three (69.6%) patients met the study inclusion criteria. 91patients (55.8%) were allocated to the intervention group. Mean days before JJ removal for intervention and control groups (“per-protocol” group) were 8.08 ± 1.52 and 8.57 ± 1.58, respectively (P = .09). There was no difference between groups regarding major urologic compli- cations (P = .679). Visual analog scale pain scores were significantly higher in the control group (p = .001). The procedure reduced 63-120 USD from the cost of operation in the intervention group. Conclusion: In selected kidney transplant patients, attaching stent to the Foley catheter and removing both of them early may be a safe maneuver regarding major urological complications, reduces pain, and eliminates the cost of cystoscopy. Keywords: cystoscopy; double-J-stent; kidney transplantation; stent; ureteric stenting INTRODUCTION With the current adequate immunosuppression, the surgical complications are the significant cause of graft loss after kidney transplants(1). Urologic compli- cations are associated with significant morbidity, graft loss, and mortality(2). The urinary anastomosis tech- nique evolution occurred gradually during more than half a century from uretero-ureteral to the ureteroneo- cystostomy anastomosis, and from Leadbetter-Politano to the Lich-Grégoire(3). The Lich-Gregoire extravesical technique has reduced these complications(4), has stood the test of time,(5), and it is technically less demanding(6). Stents which mostly are used in the Lich-Gregoire ure- teroneocystostomy(6) technique are still a controversial issue(6). The benefits of stents are still debated(6) but may include making watertight ureteroneocystostomy anastomosis procedure easier and lowering the chance of kinking(6). The optimal stent caliber, length, design(6), duration(7), and methods to remove it remain to be de- termined(6). There is a considerable amount of research about the stents to address their cost-effectiveness(8,9), their disadvantages regarding urinary tract infections(6), encrustation, reflux(10), obstruction(11), irritation, migra- tions, a dread complication of “forgotten stents” and the last but not the least, the need for the cystoscopy for 1Shahid Labbafinejad Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Urology and Nephrology Re- search Centre, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 2Resident in General Surgery, Shiraz, Iran. *Correspondence: Shahid Labbafinejad Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Urology and Nephrology Research Centre, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Received July 2019 & Accepted January 2020 their removal(12-16). Attaching ureteral stent to the Foley catheter and excluding cystoscopic removal of the stent, was first reported in 1988(17). Although it has not adopt- ed widely, we think that it is a good maneuver making transplant a more comfortable experience for patients. To the best of our knowledge, our study is the first randomized controlled trial which evaluates the major urologic complications (MUC), pain, and costs between regular stent removal through cystoscopy with stent re- moval through attachment to Foley catheter. MATERIALS AND METHODS Study design We did a randomized controlled trial in patients trans- planted at Shahid Labbafinejad Medical Center, Teh- ran, Iran (a quaternary referral hospital) from March 2016 to June 2017. The Ethics Committee of the Urolo- gy and Nephrology Research Center of Shahid Behesh- ti University of Medical Sciences approved the study protocol (IR.SBMU.UNRC.1395.13). The study has been registered in the Iranian Registry of Clinical Trials (IRCT20100313003547N6). Written informed consent obtained from all participants. The stent of all partici- pants proposed to be removed around the seventh post- op day. In the intervention group, the stent was attached to the Foley catheter by a nylon suture and removed Urology Journal/Vol 17 No. 2/ March-April 2020/ pp. 173-179. [DOI: 10.22037/uj.v0i0.5448] together. In the control group, the stent was removed by flexible or rigid cystoscopy in the operating room. Participants Eligible participants were patients 16 years and older listed for renal transplantation in the renal transplant department, which had given written informed consent. The exclusion criteria were benign prostatic hyperpla- sia causing bladder outlet obstruction, neurogenic blad- der, history of urinary diversion, history of surgery in urethra or bladder, repeat transplanations, patients who had a high risk of bleeding after reperfusion and before performing ureteroneocystostomy anastomosis, double Kidney Transplantation 174 Table 1. Etiology of the 71 patients excluded from the study. Exclusion criteria Number (%) Age less than 16 years 23 (32.3) History of BPH and bladder outlet obstruction 10 (14.0) Multiple arteries in allograft 6 (8.45) Neurogenic bladder 6 (8.45) Surgeon preferred not to included after reperfusion 3 (4.22) Up-side-down transplant of the right-sided living donor nephrectomy 3 (4.22) Sever iliac vein adhesion found during surgery 3 (4.22) Third transplant 3 (4.22) History of cystoplasty 2 (2.86) Double ureter in allograft 2 (2.86) Double ureter and multiple arteries in the allograft 2 (2.86) Transplant in continent urinary diversion 1 (1.40) Iatrogenic trauma to the allograft ureter leading to Boari flap procedure 1 (1.40) History of vesicostomy and Mitrofannoff procedure 1 (1.40) Others 3 (4.22) Variablesa Modified intention-to-treat group (%) Per-protocol group (%) Intervention group Control group P value Intervention group Control group P value Randomiza-tion Per-protocol 73 (80.2) 50 (69.4) .016 NA NA NA As-treated 6 (6.6) 1 (1.4) NA NA NA Intention-to-treat 12 (13.2) 21 (29.2) NA NA NA Age 43.85 (±15.09) 41.42 (±14.25) .311 44.66 (±14.39) 37.91 (±13.95) .013 Sex Male 53 (58.9) 45 (63.4) .562 46 (63.0) 32 (64.0) 1 Female 37 (41.1) 26 (36.6) 27 (37.0) 18 (36.0) BMI 24.83 (±4.56) 25.0 (±4.15) .821 24.93 (±4.07) 24.02 (±4.21) .505 Etiology DM 18 (19.8) 11 (15.3) .108 15 (20.5) 6 (12) .219 HPT 19 (20.9) 12 (16.7) 14 (19.2) 8 (16) Unknown 15 (16.5) 10 (13.9) 13 (17.8) 8 (16) Preemptive 20 (25.3) 15 (22.7) .717 18 (27.3) 9 (19.1) .375 Dialysis dura-tion 16.57 ((±22.5) 15.61 (20.17) .787 14.71 (±20.2) 17.06 (±22.15) .557 Positive Histo-ry of diabetes 21 (25.9) 12 (17.1) .238 17 (27) 6 (12.5) .097 Donor Live 44 (48.4) 31 (43.7) .332 38 (52.1) 24 (48.0) .398 Cadaveric 47 (51.6) 40 (56.3) 35 (47.9) 26 (52.0) Previous his-tory of trans-plant No 67 (87.0) 58 (90.5) .345 54 (87.1) 44 (95.7) .117 Yes 10 (13.0) 6 (9.4) 8 (1209) 2 (4.3) Donor age 34.1 ((±11.89) 33.91 ((±11.03) .920 33.83 (±11044) 31.35 (±9.69) .220 Donor sex Male 65 (78.3) 44 (64.7) .175 54 (80.6) 32 (66.7) .234 Female 17 (20.5) 23 (33.8) 12 (17.9) 15 (66.7) Left or right Right kidney 24 (27.3) 22 (32.4) .596 15 (21.4) 13 (27.1) .311 Left kidney 64 (72.7) 46 (67.6) 55 (78.6) 35 (72.9) Warm ische-mia time 2.62 ((±3.09) 2.80 ((±3.34) .799 2.87 (±3.07) 3.33 (±3.45) .571 Cold ischemia time 117.04 ((±79.07) 112.33 ((±66.01) .781 103.58 (±69.81) 97.70 (±66.77) .758 Surgeon’s ex-pertise level Senior cosultatn 35 (39.3) 19(27.5) .272 27 (37.5) 13 (27.11) .237 (NS, AB, AT) Jonior consultant (MNS) 12 (13.5) 13 (18.8) 10 (13.9) 12 (25) Surgical fellow 42 (47.2) 37 (53.6) 35 (48.6) 23 (4709) Day double J removed 8.93±3.87 11.79±6.69 .001 8.08 (±1.52) 8.57 (±1.58) .094 Immunosuppression Cyclospor-ine+Mycophenolic 33 (53.2) 29 (46.8) .767 27 (56.3) 21 (43.8) .745 acid + Corticoster-oids Tacro +Mycophenolic acid 24 (58.5) 17 (41.5) 19 (63.3) 11 (36.7) + Corticosteroids Cyclosporine + Si-rolimus 7 (43.8) 9 (56.3) 6 (54.5) 5 (45.5) + Cortico-steroids Tacro + Sirolimus + Corticosteroids 12 (50) 12 (50) 9 (47.4) 10 (56.3) Table 2. demographic characteristics and immunosuppression regimens. Double-J Stent in Kidney Transplant-Nadjafi-Semnani et al. ureter, or multiple arteries in the allograft, and any in- juries to the vessels or ureter during retrieval (Table 1). Randomization The patients were randomly allocated (1:1) to either at- taching the stent to the Foley catheter or not attaching them during transplant. A computerized randomiza- tion list in blocks of five in random order was created. Numbered dark pockets containing the study groups (attached or not attached) were prepared and sealed ac- cordingly. After reperfusion, if the surgeon did not have any contraindication for allocating the patients, rand- omization to the intervention or the control groups was done. There was no blinding. Procedures The technique of Lich-Gregoire extravesical anastomo- sis has been described elsewhere(12,18). The anastomosis was done using 5/0 polyglactin suture. The Foley cathe- ter was attached to the stent with 3/0 nylon stitch, which was passed through the distal end of the stent and the distal drainage eye of the catheter. All patients received Cotrimoxazole for six months. Outcomes The primary outcome was a urinary leak or a ureteric obstruction treated with intervention and was defined as major urologic complications (MUC). Secondary outcomes were pain experienced by the patients during stent removal and the reduction of the cost of kidney transplantation. The data were collected by completing a questionnaire. Statistical analysis The primary analysis was targeted to the “modified in- tention-to-treat” group, although we did the “per-pro- tocol” analysis for cases with no significant protocol violations as well. Pearson's chi-squared test, Fisher’s exact test, Independent-samples T-test, One-way ANO- VA were used for analysis. Non-parametric Mann- Whitney U test was used for visual analog score anal- ysis. Throughout, we reported two-sided p values. A P value of less than 0.05 was considered significant. We used SPSS software (version 22.0) for the statistical analysis. RESULTS From March 2016 to June 2017, two hundred thir- ty-four patients, mean age 40.11 ± 17.06 (6-77) years; 121 (51.7%) from deceased donors, were transplanted in our department; Seventy-one patients did not meet the inclusion criteria (Table 1). One hundred six- ty-three patients were randomly allocated to either an intervention group (n = 91) or control group (n = 72) (Figure 1). There were no differences in demograph- ic characteristics between the two groups (Table 2). Mean time to stent removal in the intervention and control groups were 8.93±3.87(CI95%: 8.09-9.77), and 11.79 ± 6.69 (CI95%: 10.07-13.50), respectively (P = .001). One hundred twenty-three patients whose stent were removed early from six to fifteen post-op days were considered as protocol cases and analyzed as a “per-protocol” group. Thirty-three patients violat- ed the protocol significantly and were analyzed as an “intention-to-treat” group (Table 3). In 16/163 (9.8%) patients, the catheter was removed after 15th post-op day by the decision of the in-charge surgeon because of their post-op condition such as delay graft function. In 33 patients who substantially broke the protocol, the mean ureteric stent removal day in intervention and control groups was 12.75 and 22.38 days (P = .008), re- spectively. Seven randomized patients were considered “as-treated” group because they should not have been included in the study (Table 4). The sum of “inten- tion-to-treat,” “as-treated,” and “per-protocol” groups were defined as 163 cases of the “modified inten- tion-to-treat” group. Because from March 2016 to Janu- ary 2017, attaching the stent to catheter was satisfactory in adults, from January 2017, NS and MNS were attach- ing the ureteric stent to the Foley catheter in all of their pediatric transplantations. These caused the residents in our department to consider three children as included in the study by mistake, and the parents of three pediatric patients aged 8, 14, and 15 years, were asked to give the informed consent and were randomized inadvertent- ly to the intervention group. One of these three cases, an eight years old girl, developed urinary leakage af- ter stent removal on the 7th post-op day and underwent ureteroneocystostomy three days later. Six patients in the “per-protocol” group had their catheter removed on the six post-op day. 3/91 (3.2%) patients had accidental stent dislodgement due to malfunction of the balloon of the Foley catheter, (two on the third and one case on the fifth post-op day), and none of them developed MUC, although one of them developed lymphocele. 5/163 (3%) cases, including 3/91 (3.2%) in the in- tervention and 2/72 (2.81%) in the control group un- derwent ureteroneocystostomy after transplant. 4/163 (2.4%) cases had a urinary leakage, which was resolved by short term percutaneous drainage. One of these four cases was treated by both a percutaneous nephrostomy along with percutaneous drainage. There was no sig- nificant difference between the intervention and control Reason for meeting the exclusion criteria Number Age less than 16 years 3 Multiple arteries in allograft 3 Neurogenic bladder 1 Table 3. Description of the patients included in the “as-treated” group Reasons for violation of the protocol Numbers Foley catheter came out accidentally before the six post-op day 3 The in-charge surgeon preferred to delay removal for a reason like a delay graft function, rejection, 16 Arterial/venous thrombosis or severe rejection leading to graft nephrectomy 5 Postoperative hemorrhage and exploration for hematoma evacuation 4 High output drain due to urinary leak and lymphocele 2 Severe hyponatremia and convulsion 1 The patient expired before removing the catheter 1 Nonfunctioning graft due to arterial thrombosis 1 Total 33 Table 4. Description of the patients analyzed as “Intention-to-treat” group. Double-J Stent in Kidney Transplant-Nadjafi-Semnani et al. Vol 17 No 02 March-April 2020 175 groups regarding the MUC (Table 5). The cost of cys- toscopy with and without general anesthesia was 120 and 63 USDs respectively, which was eliminated in the intervention group. DISCUSSION To our knowledge, this is the only randomized study in which the attachment of the ureteric stents to Foley catheters versus cystoscopy removal of ureteral cath- eters were compared in early stent removal groups. 5/163 (3%) patients had ureteroneocystostomy, and 4/163 (2.4%) patients had leakage which was resolved by insertion of a percutaneous drain with or without a nephrostomy. MUC in our previous study of 100 KT patients in whom urethral catheter was attached to ureteral stent and removed together three weeks after transplanta- tion was 4% (one stenosis and three fistulas)(12). Patel et al.(19), in a randomized trial conducted at six trans- plant centers in the UK, studied 205 patients aged 2 to 57 years old. Cases were randomized to early removal arm, in which stent was attached to the Foley catheter and were both removed at the 5th post-op day and a late removal arm, in which stent was removed at six weeks with cystoscopy. 3/80 cases (3.75%) in early removal group and 1/126 (0.79%) in late removal group; (P = 0.36) had ureteroneocystostomy(19). Stent complications occurred in 27.3% and 10% in late and early stent re- moval groups, respectively; (P = .387). Urinary tract infection in the early and late groups occurred in 7.6% Kidney Transplantation 176 Table 5. Outcomes comparison between intervention and control group. Modified intention-to-treat group Per-protocol group Vairablesa Intervention group Control group P value Intervention group Control group P value Stent dislodgement 3 (3.8) 0 .252 0 0 Urinary leak 6 (8.0) 2 (4.1) .477 4 (4.1) 2 (4.8) 1 Lymphocele 1 (1.3) 1 (1.7) 1 0 0 Ureteroneocystostomy 3 (3.3) 2 (2.8) .849 2 (2.7) 1 (2.0) 1 Drain for collection 3 (3.4) 1 (1.4) .627 3 (4.1) 1 (2.0) 0.645 Nephrostomy for hydronephrosis 1 (1.1) 0 1 1 (1.4) 0 1 Major urologic complications 5 (5.5) 3 (4.2) .679 5 (6.8) 2 (4.0) 0.7 Visual analoge scaleb score .35 (IQR.6 ) 4 (IQR 6.35) .000 4 (IQR .7) 3 (IQR 6.2) .001 Follow up 283 ± 132 296 ± 131 .545 299.7 (±126.8) 319.9 (±124.3) 0.393 Mean creatinine one year after 1.30 ± .46 1.22 ± .37 .247 1.29 (±.44) 1.22 (±.38) 0.411 transplant a Continuous variables were compared by independent samples t-test b Continuous variables were compared by Mann Whitney U test Figure 1. Trial profile. Double-J Stent in Kidney Transplant-Nadjafi-Semnani et al. and 24.6%, respectively; (P = .004). 37 (18%) patients were ≤ 16 years, and there was no ureteroneocystosto- my in any(19) patient. In 11 patients, the surgeon was not able to attach the stent to the urethral catheter because it was a little bit challenging task(19). We also acknowl- edge that finding the catheter and extracting it through a small incision of bladder mucosa is challenging. One of the authors’ recommendations (NS) for this issue is to push the bladder downward so that the superior bladder wall approaches to the floor of the bladder. By this maneuver, the tip of the Foley catheter could be grabbed quickly and smoothly by the surgeon. In a retrospective study (2007-2009 ) in the UK(20) on 127 transplantation comparison was made between 48 cases, which their ureteric stents were removed on the 5th post-op day with 79 cases in which their stents re- moved 6-8 weeks postoperatively by flexible cystosco- py. UTI occurred in early and late removal groups in 25% and 44% (P = .03), respectively. MUC in early and late removal groups were 4% and 7% (P = 1), re- spectively. The preliminary result of an ongoing randomized trial comparing early with late stent removal in adults (IS- RCTN51276329) has revealed that MUC has not in- creased in the early group (Mr. Kourosh Saeb-Parsy. Addenbrooke's Hospital (UK), November 2018, email response). Sansalone et al.(21), in 590 consecutive transplanted pa- tients, attached the 7 or 8 Fr silicone ureteral stent to the Foley catheter and removed both together at mean duration of ten days(8-14). Urinary leakage and stenosis occurred in 0.3% and 1.5% respectively(21). In 1998, the simple technique of attaching the ureteric stent to the Foley catheter was reported for the first time by Morris-Stiff (a surgical research fellow) et al.(22) In fifteen (eight men) patients, mean age 48 years, they have attached the stent to a Foley catheter and removed both at the mean eight post-op day. None of them devel- oped MUC or sepsis. The authors conclude the method as a useful maneuver to be used in renal transplantation. Authors state that they had not invented, but they have reported this technique in the surgical literature(22). Baxbi, k.(23) (a consultant urological surgeon) wrote a re- markable letter to the journal and criticized the authors’ conclusion as follow: “ authors describe a method of suturing the distal end of a ureteric stent to the tip of the urethral catheter at the time of ureteric anastomosis and say that they cannot find this technique described in the surgical literature. Perhaps the reason for the lat- ter is that orthodox urological teaching has long been that this is bad practice. The reason is that if the ure- thral catheter is, or has to be, removed very early in the postoperative period, the ureteric stent inevitably comes with it. The catheter may block with clots (admitted- ly rare after transplantation) and have to be changed; a faulty balloon may deflate so that the catheter 'falls out while the bed is being changed,' and it is not unknown for a confused patient to remove the urethral catheter with the balloon intact(23).” The comments by Bixbi are a real and annoying concern for every transplant sur- geon. In 3/92 (3.26%) of our patients, the catheter came out for the faulty balloon, and none of them developed MUC. All of them were re-catheterized, and the cath- eter removed from 7th to 10th post-op day, although one of them developed lymphocele. Patel et al(19). re- ported catheter and the ureteric stent attached to it were dropped out before the fifth post-op day in 2/79 (2.53%) cases, which is in concordance to our study. Parapiboon et al.(24), in a randomized study of 74 pa- tients, assessed the MUC and UTI in two groups in which the stents were removed either on the median of 8 or 15 days. UTI and MUC in the eight days and 15 days were 40.5% vs. 72.9%; (P = .004) and 2 cases vs. 4 case; (P = .39) respectively(24). Taghizadeh et al.(25) reported the result of a prospec- tive study randomizing 43 cases to a cystoscopic stent removal group at four post-op week and another 43 pa- tients to the attachment of Foley to the ureteric stent group removed at seventh post-op day. The UTI and Urinary leak in early and late removal groups were not significantly different(25). Impressing innovations in KT have reported for omit- ting the cystoscopy, the unwanted procedure imposed by the use of the stent(26,27). As an exciting innovation, the magnetic-tipped stent was first introduced by Ma- caluso et al. in 1989(28) and was developed mainly to decrease additional costs associated with stent removal. Pain measurement by Visual analog scale method in our study showed that cystoscopic stent removal was signif- icantly more painful than removal by pulling the Foley catheter, which is attached to the stent. In a study of the pain at stent removal in the USA, 68 patients who un- derwent ureteroscopy for urolithiasis were randomized to stent removal by office cystoscopy or the removal by pulling an attached string. The pain score was lower in the cystoscopic removal as compared to removing it by pulling the string, although the difference was not significant(29). There are some shortcomings in our research. First, the data provided is from a single center with center-specific patients, treatment protocol, and a financial perspective. We have excluded 23 children from our study, although no evidence shows a younger age of the recipient is a more significant risk factor for MUCs. We did not study the UTI in our trial. Although both groups in our study had an equal indwelling stent time, i.e., eight days, but its measurement could reveal the effect of cystoscopy on the occurrence of UTI in transplanted patients. In- sertion of the stent is easy but will add a procedure of cystoscopy to the KT, for its removal. Cystoscopy after kidney transplant unquestionably increases the risk of UTI. There are reports of urosepsis in the transplanted immunocompromised patients after cystoscopy(30). Our study has an insufficient sample size. However, ours is the most extensive reported series of its sort. Moreover, the study was not able to blind the surgeons or patients regarding the allocation. Notwithstanding the previously mentioned shortcom- ings, we could analyze the primary outcome in the intention-to-treat subgroup and compare it with the per-protocol group. Our randomized clinical study presents a shred of clear evidence regarding the rate of MUCs occurring with the early stent removal strategy in 163 patients. MUC is the critical concerns of sur- geons wishing to remove the stent early by attaching the ureteric stent to the Foley catheter. The attaching ureter- ic stent to the Foley catheter is not practiced widely and not a well-acknowledged strategy in KT, although it is an easy-to-do maneuver. It is clear from our trial that this is a safe and economical procedure with less pain for the patients in regards to omitting the cystoscopy for the stent removal. Double-J Stent in Kidney Transplant-Nadjafi-Semnani et al. 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