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1 E U R O P E A N U R O L O G Y F O C U S X X X ( ) X X X X X X ava ilable at journa l homepage: nurology.com/eufocus Stone Disease Outcomes of Elective Ureteroscopy for Ureteric Stones in Patients with Prior Urosepsis and Emergency Drainage: Prospective Study over 5 yr from a Tertiary Endourology Centre Amelia Pietropaolo a, Jane Hendry b, Rena Kyriakides a, Robert Geraghty a, Patrick Jones a, Omar Aboumarzouk b, Bhaskar K. Somani a,c, * a University Hospital Southampton NHS Trust, Southampton, UK; b Glasgow Urological Research Unit, Department of Urology, Queen Elizabeth University Hospital, Glasgow, UK; c University of Southampton, Southampton, UK Article info Article history: Accepted September 5, 2018 Associate Editor: Richard Lee Keywords: Nephrostomy Outcomes Sepsis Stent Stone Ureteroscopy Abstract Background: Elective treatment of ureteric stones is needed after emergency drainage of urosepsis. Objective: We wanted to look at the outcomes of elective ureteroscopic stone treatment in patients with prior sepsis and emergency drainage via retrograde ureteric stent (RUS) or percutaneous nephrostomy (PCN). Design, setting, and participants: Data of all patients who underwent elective ureteroscopy (URS) for stone disease over 5 yr (March 2012 December 2016) were prospectively collected. Intervention: Elective URS following previous emergency RUS or PCN. Outcome measurements and statistical analysis: Outcomeswerecollatedforconsecutivepatientswho underwent emergency drainage for urosepsis secondary to stone disease, followed by elective URS. Data was collected regarding patient demographics, stone parameters, and clinical outcomes. Statistical analysis was performed using SPSS version 24. Results and limitations: In total, 76 patients underwent 82 elective procedures (six underwent bilateral URS) with a male to female ratio of 1:2 and a mean age of 57 yr. Emergency decompression was achieved via RUS in 63 (83%) and PCN in 13 (17%) patients. A positive urine culture on presentation was obtained in 26 (34%) patients, and 27 (36%) patients were admitted to the intensive care unit (ICU). The mean single and overall stone size was 8.6 (2 23) and 10.8 (2 32) mm, respectively. The mean operating time was 42 (5 129) min with stone-free rate (SFR) of 97% (n = 74). There were three (4%) complications in total, of which two patients developed urinary tract infection needing intravenous antibiotics (Clavien II) and a third developed sepsis (Clavien IV) needing ICU admission. There was no difference in ureteroscopic lithotripsy outcomes (operative time, complications, or SFR) on comparing initial RUS or PCN, admission to ICU or ward, positive or negative urine culture result, presence of single or multiple stones, and between American Society of Anaesthesiologists (ASA) grade of patients. The ASA grade of patients was a significant predictor of day case procedures (p = 0.001). Conclusions: Elective URS achieved excellent outcomes in patients who previously presented with obstructing calculi and sepsis needing emergency decompression. Overnight inpatient admission was needed in some patients with a higher ASA grade. Patient summary: In this report, we look at the outcomes of planned ureteroscopy procedures for stone disease in patients with previous urosepsis. These patients with previous emergency drainage for urosepsis had excellent outcomes from their planned ureteroscopic surgery. This information will help in preoperative patient optimisation and counselling European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Department of Urology, University Hospital Southampton NHS Trust, SO16 6YD, Southampton, UK. Tel ; Fax: address: b.k.somani@soton.ac.uk (B.K. Somani) / 2018 European Association of Urology. Published by Elsevier B.V. All rights reserved.

2 2 E U R O P E A N U R O L O G Y F O C U S X X X ( ) X X X X X X 1. Introduction Kidney stone disease prevalence has risen over the last two decades due to increase in metabolic syndrome, changes in weather with global warming, and incidental stones picked up on imaging [1,2]. This has led to more patients presenting with colic, haematuria, urinary tract infection (UTI), and some with urosepsis due to infected obstructed kidneys secondary to ureteric or renal stones [3 6]. Ureteric obstruction as a result of calculi is recognised to be a cause of severe sepsis in 10% of patients presenting with sepsis [6]. In infected obstructed kidneys leading to sepsis, the initial management is directed towards aggressive fluid resuscitation, antibiotic therapy, hemodynamic support, and controlling the source by drainage of the infection [4 7]. Urgent surgical decompression of the urinary tract obtains source control and is crucially associated with a decreased mortality, which can be a sequela of sepsis [4,6]. Whilst ureteric stenting or a percutaneous nephrostomy (PCN) relieves the obstruction, definitive management of the stone is subsequently required at a later stage. Once urosepsis is treated by emergency drainage, upon recovery, elective treatment of the underlying stone is necessary. We wanted to look at the outcomes of elective ureteroscopic stone treatment in these patients with prior sepsis and emergency drainage. Specifically, we compared the operative time, complications, and stone-free rate (SFR) in patients with initial retrograde ureteric stent (RUS) or PCN, admission to intensive care unit (ICU) or ward, previous positive or negative urine culture, presence of single or multiple stones, and between American Society of Anaesthesiologists (ASA) grade of the patients. In addition, we wanted to identify any risk factors for developing complications and predictors for day case ureteroscopy (URS). 2. Patients and methods Data of all patients who underwent URS for stone disease over a 5-yr period (March 2012 December 2016) were collected in our prospective database. Our audit was registered with our hospital Clinical Effectiveness team, with patient consent obtained for participation in the study [8,9]. Outcomes were collated for consecutive patients (>14 yr) who underwent emergency drainage for urosepsis secondary to stone disease, followed by elective URS 6 12 wk post recovery. The procedures were performed or supervised by a single experienced endourologist (BS). Data was then cross-checked and analysed retrospectively by a third party (A.P., R.K.) not involved in the original procedure. During the initial episode of sepsis, all patients were screened for high or moderate risk of sepsis with an immediate resuscitation [7]. Patients were assessed by a member of outreach or critical care team, and depending on the severity of sepsis, they were either transferred to ICU or kept in high-dependency unit or ward under close observations. Apart from their routine observations (alertness, temperature, skin colour and turgor, respiratory rate, blood pressure, heart rate and urine, output), patients also had their serum inflammatory markers, such as white blood cells (WBC) and C-reactive protein (CRP), and renal function measured. The initial assessment of urosepsis was based on patient s assessment of vital signs (heart rate, respiratory rate, and temperature) blood pressure, oxygen saturation, level of consciousness, urine output/frequency over last 18 h, and skin turgor/colour [7]. Other diagnostic tests included microbiological (urine and blood culture), biochemical (WBC, CRP, serum lactate, and arterial blood gas) and radiological (ultrasound scan [USS] and/or computed tomography scan), which not only helped in assessment but also in guiding on-going management [7]. Broad-spectrum antibiotics were initially used in conjunction with emergency drainage of obstructed infected kidney. These were subsequently tailored to microbiology results along with clinical and biochemical response. Emergency surgical drainage was performed either via RUS insertion or PCNdrainage. On complete recovery, a planned elective URSwas scheduled for these patients. Upon discharge, patients were re-assessed regarding their fitness for surgery at a dedicated anaesthetist-led pre-assessment clinic [8,9]. All microbiology results were re-evaluated, and antibiotic prophylaxis for surgery was checked. In case of negative urine culture, a standard protocol-based perioperative antibiotic was given. For culturepositive patients, either appropriate preoperative antibiotics were started 5 7 d prior to the procedure, or for high-risk patients with resistant organisms, this was done in conjunction with the microbiology team. Using a day case procedure protocol and a standard surgical technique for URS and laser stone treatment described previously [9], most patients were planned for discharge the same day or the following morning. With a safety guidewire in place, a semi-rigid URS (4.5 F or 6 F Wolf or Storz ureteroscope) was performed first, followed by a flexible URS (Storz FlexX2), and stones were managed by either laser fragmentation, basket extraction, or a combination of these two. Data was collected on patient demographics including comorbidities and ASA grade, stone parameters (mm), previous microbiology results, preoperative and postoperative WBC (10 9 /l) and CRP (mg/l), operative time (min), use of ureteral access sheath, postoperative stent and urethral catheter use, length of stay (d), stone analysis, complications, and SFR. SFR was defined as 2U or 2X [10], being complete disappearance or clinically insignificant fragments 2 mm on USS or kidney, ureter, and bladder X-ray on follow-up. Postoperative complications were recorded as per the Clavien-Dindo classification [11]. Statistical analysis was performed using SPSS version 24. Continuous independent variables were tested using independent samples t test, paired samples were tested with paired t test. Dichotomous data were tested using chi-square test or Fisher s exact test (FET), if one of the counts was less than five. Graphs were generated in SPSS. Results of t test are displayed with p values and 95% confidence intervals (CI), and chisquare and FET results are displayed as p values. 3. Results A total of 76 patients underwent 82 elective procedures (six underwent bilateral URS) with a male to female ratio of 1:2 and a mean age of 57 yr (range, yr; Tables 1 and 2). All patients came with urosepsis, and 27 (36%) patients required admission to ICU [12]. The mean pre-procedure WBC count and CRP was 14.4 (2.7 42) and (1 425), respectively. Emergency decompression was achieved via RUS in 63 (83%) patients and PCN in 13 (17%) patients. The median time interval between initial RUS or PCN during the urosepsis episode and their elective URS lithotripsy (URSL) was 60 d (7 250 d). A positive urine culture on presentation was obtained in 26 (34%) patients. The organisms grown were Escherichia coli (n = 20, 77%), yeast (n = 3, 12%), and one patient each grew Pseudomonas, group B Streptococcus, and Proteus mirabilis, respectively. The mean single and overall stone size was 8.6 (2 23) and 10.8 (2 32) mm. The stone location was in the ureter (n = 45, 59%), both ureter and kidney (n = 17, 22%) or in the

3 E U R O P E A N U R O L O G Y F O C U S X X X ( ) X X X X X X 3 Table 1 Patient demographics and clinical outcomes. Patient demographics and preoperative parameters (76 patients, 82 procedures) Male:female (n) 25:51 Mean age, yr (range) 57 (14 86) Side (n) right:left:bilateral 37:33:6 ICU admission:non-icu admission, n (%) 27 (36):49 (64) Mean preoperative WBC (range) 14.3 (2.7 42) Mean preoperative CRP (range) 199 (1 425) Urine growth, n (%) 26 (34) Retrograde stent:nephrostomy:antegrade stent, n (%) 63 (83):13 (17) Stone parameters, outcomes, and postoperative parameters Mean stone size, mm (range) Cumulative stone size, mean, mm (range) 8.6 (2 23) 10.8 (2 32) Stone location isolated ureteric:multiple, n (%) 45 (59):31 (41) Ureteral access sheath, n (%) 14 (19) Mean operating time (min) 42 (5 129) Postoperative stent placement, n (%) 70/76 (92) Postoperative urethral catheter placement, n (%) 25 (33) Stone-free rate, n (%) 74/76 (97) Mean postoperative WBC (range) 8 ( ) Mean postoperative CRP (range) 20.7 (<1 76) Length of stay, d 0 60 (79%) 1 7 (9%) >1 9 (12%, range: 2 35) Complications (2 Clavien II, 1 Clavien IV) 3/76 (4%) 2 UTI needed IV antibiotics 1 urosepsis needed ICU admission CRP = C-reactive protein; ICU = intensive care unit; UTI = urinary tract infection; WBC = white blood cell. Table 2 Effect of different variables on outcomes (operative times, complications, stone free rate, procedures done as a day case). Operative time, p value (95% CI) Complications, (p value) SFR, (p value) Day case procedures, (p value) Retrograde ureteric stent versus nephrostomy 0.13 ( 28.9 to 3.6) ICU versus ward 0.77 ( 11.6 to 15.8) Negative versus positive urine culture 0.13 ( 3.1 to 23.7) No access sheath use versus access sheath use (5.3 to 31.6) Single versus multiple stones 0.25 ( 26.7 to 7.0) ASA I/II versus ASA III/IV 0.12 ( 23.0 to 2.7) ASA = American Society of Anaesthesiologists; ICU = intensive care unit; SFR = stone-free rate. kidney (n = 14, 19%). The ureteric location was vesico-ureteric junction (n = 5), distal ureter (n = 16), mid ureter (- n = 8), proximal ureter (n = 11), pelvi-ureteric junction (- n = 5), and impacted renal pelvic stone (n = 5). The mean operating time was 42 (5 129) min with SFR of 97% (n = 74). Post procedure, the urethral catheter was removed after h and the RUS after 1 3 wk. There were three (4%) complications in total, of which two patients developed UTI needing intravenous antibiotics (Clavien II). One patient with a history of multiple sclerosis with a previous yeast infection and ICU admission developed Clavien IV complication and was readmitted to ICU postoperatively with sepsis. However, a complete recovery was made with treatment and the patient was subsequently discharged home. The ASA grades of the included patients were ASA I (n = 17), ASA II (n = 26), ASA III (n = 28), and ASA IV (n = 5), with 18 (24%) patients having diabetes mellitus and 34 patients with two or more than two comorbidities. The stone analysis results were available in 57 (75%) patients. Of the patients with available stone analysis, calcium oxalate stones were seen in 40 (70%), struvite stones in 12 (21%), and uric acid in four (7%). There was no difference in URSL outcomes (operative time, complications, or SFR) on comparing initial RUS or PCN, admission to ICU or ward, positive or negative urine culture result, presence of single or multiple stones, and between ASA grade of patients (Table 2). However, the operative time was significantly shorter for patients without the use of ureteral access sheath (p = 0.007). The ASA grade of patients was a significant predictor of day case procedures, and patients with lower ASA grade were more likely to be undergo a day case procedure (p = 0.001). However, urine culture, multiplicity of stones, and presence or absence of complications were not predictors of day case procedures. There was a significant decline in WBC count and CRP of patient s post-drainage of infected obstructed kidneys (p < 0.001; Fig. 1). 4. Discussion 4.1. Meaning of the study Our study highlights the safety and efficacy of elective URS in patients with previous sepsis from obstructing ureteric

4 4 E U R O P E A N U R O L O G Y F O C U S X X X ( ) X X X X X X Fig. 1 Difference between C-reactive protein and white blood cell count from initial admission to discharge. CI = confidence interval; CRP = C-reactive protein; WBC = white blood cell. calculi. Immediate drainage of sepsis with delayed treatment of underlying stone achieved an excellent SFR with morbidity similar to that mentioned in large non-urosepsis URS series [13]. Despite being a high-risk non-selective cohort with 33 (45%) being ASA III, the patients had good clinical outcomes with three-quarters of all patients being discharged the same day. A high rate of postoperative RUS and urethral catheter insertions was done to minimise the potential rates of sepsis and to maintain a good drainage from the upper urinary tract. Patients with lower ASA grades were more likely to be discharged home the same day than those with higher ASA grades Comparison of our study to what is known in the literature Management of infected obstructed kidneys can be achieved by a RUS or PCN. A similar study looking at a time trend analysis over 11 yr ( ) from a nationwide inpatient sample (NIS) in USA showed a rising trend of infected urolithiasis and associated sepsis [6]. The study also found that women were twice as likely to have infected urolithiasis, and there was a decreasing use of PCN over time. Sub-analysis of data based on sepsis and emergency admissions also showed slightly favourable outcomes of RUS versus PCN [6]. Urosepsis-related mortality was higher (2.5 times) in patients with urinary obstruction [14]. Overall, of all patients with urinary source of septic shock, 10% were due to urinary obstruction of which 77% were related to urolithiasis. Urgent resuscitation and early source control with decompression of obstruction is the key to avoiding mortality [14]. In another NIS sample study from USA, mortality was significantly higher in patients with calculi-related sepsis where surgical drainage was not carried out with mortality twice as high compared to when RUS or PCN was performed [3]. Although the timing of drainage was not clear, early drainage within 2 d was shown to reduce the overall length of hospital stay [15]. In a similar Japanese study, where 59 emergency drainages were done for urosepsis secondary to stone disease, 59% and 41% underwent RUS and PCN, respectively [16]. Previously, a retrospective matched-pair comparison between elective URS and patients with prior urosepsis showed a significantly higher complication rate (20%) and longer length of stay in the latter group [17]. With 69 patients in each group, the SFR, hospital stay, and high-grade complications in elective patients, and patients with prior urosepsis were 77% and 81%, 0.6 and 2.5 d, and 4% and 7%, respectively. Compared with this, in our prospective study, the SFR was 97% and there was only one high-grade complication. The choice of RUS or PCN has often been debated with no clear answers to date [18,19]. Although theoretical risk of increased pelvicalyceal pressure and worsening sepsis have been proposed with RUS, no conclusive evidence or guidance is available to date. The important aspect is to establish drainage urgently otherwise the outcomes are sub-optimal and potentially could lead to patient mortality. In our series, considering one third of patients were admitted to ICU with ventilatory support, it was easier to perform RUS in supine lithotomy position without the need for a prone positioning for a PCN. No differences in outcomes were noted for RUS or PCN or whether the patient was admitted to the ICU or the ward Strengths and limitations of our study Our study was conducted in a prospective manner for consecutive patients who had emergency drainage followed by elective URSL, which was performed using a standardised technique [9]. Data were collected and analysed independently by third party not involved with the original study. Statistical analysis on predictors of outcomes and length of stay was performed and presented. Although the study was done prospectively, stone burden, quality of life, or formal cost analysis was not studied. This paper describes

5 E U R O P E A N U R O L O G Y F O C U S X X X ( ) X X X X X X 5 the feasibility of urinary stone treatment in elective setting after first diversion, with morbidity similar to that mentioned in large, non-urosepsis URS series. This suggests that previous urosepsis condition, when correctly treated in the acute phase, does not influence the result of definitive treatment. The time interval between their emergency drainage and elective URS was influenced by their initial hospital stay, subsequent anaesthetic pre-assessment, and optimisation of fitness for their elective procedure with some patients with higher ASA grade waiting longer. Although we did not specifically look at the anaesthetic or surgical reasons for delay, the eventual outcomes for all patients irrespective of their ASA grades were similar, suggesting the robustness of this pathway Areas of future research In an era of growing antimicrobial resistance, it is prudent for urology units to know their local antibiotic resistance patterns [20,21]. Although work has been done on predictors of septic shock [22,23], perhaps more can be done to create awareness on prevention and prompt treatment of this condition. Previously, it has been shown that patients with indwelling stents had a higher risk of sepsis unless they underwent URS within 1 mo [24]. However, these patients underwent elective URS rather than our cohort of patients who underwent prior urosepsis. The safety of stent dwell time in these high-risk groups ought to be defined. Our study mainly focuses on ureteroscopic management of stones; however, future studies can perhaps also look at the role of minimally-invasive percutaneous techniques (eg, percutaneous nephrolithotomy) for these patients. Similarly, the time duration the patients have to wait between their emergency drainage and elective URS procedure is not defined in the literature, and studies should address this for guiding clinicians on deciding the optimal time of planned elective procedure. 5. Conclusions Elective URS achieved excellent outcomes in patients who previously presented with obstructing calculi and sepsis needing emergency decompression. Overnight inpatient admission was needed in some patients with a higher ASA grade. Author contributions: Bhaskar K. Somani had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Pietropaolo, Somani. Acquisition of data: Pietropaolo, Kyriakides. Analysis and interpretation of data: Geraghty, Jones. Drafting of the manuscript: Pietropaolo, Hendry. Critical revision of the manuscript for important intellectual content: Aboumarzouk, Somani. Statistical analysis: Geraghty. Obtaining funding: None. Administrative, technical, or material support: None. Supervision: Somani. Other: None. Financial disclosures: Bhaskar K. Somani certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None. Funding/Support and role of the sponsor: None. 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