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Modified technique for robot-assisted laparoscopic infantile ureteral reimplantation for obstructive megaureter

Open AccessPublished:May 25, 2022DOI:https://doi.org/10.1016/j.jpedsurg.2022.05.015

      Abstract

      Purpose

      To describe a novel modification of technique to improve efficacy of robot-assisted laparoscopic extravesical ureteral reimplantation (RALUR-EV) in infants.

      Materials and methods

      Between April 2017 and July 2019, sixteen infants with primary obstructive megaureter (POM) (Age range: 4–12 months) underwent robot-assisted ureteral reimplantation were reviewed in this series. In addition to the conventional Lich-Gregoir technique, the detrusor tunnel has been extended to the mobilized anterior bladder wall to guarantee sufficient tunnel length/ureter diameter ratio and avoid ureteral angulation. All patients underwent repeated ultrasound, diuretic renal dynamic imaging and voiding cystourethrography (VCUG) perioperatively and the outcomes were documented.

      Results

      All operations were completed with robotic assisted approach without conversion. Bilateral and unilateral reimplantation were respectively performed in two and fourteen patients. The mean operative time was 115.0 ± 19.5 min and the mean blood loss was 10.0 ± 1.8 ml. There were no high-grade complications (III–IV on Clavien-Dindo classification) except for one patient. The distal ureteric diameter was reduced from pre operative 1.7 ± 0.5 to 0.6 ± 0.5 cm 6 months post operatively (p < 0.05). One child (6.3%) required the second reimplantation for stenosis. The overall operative success rate was 94.4% (17 of 18 ureters) with a mean follow-up of 15.9 ± 7.4 months with no flux detected.

      Conclusion

      Our preliminary experience suggests that our modified robot-assisted laparoscopic extravesical ureteral reimplantation is feasible in infants with good results.

      Keywords

      Abbreviations:

      POM (primary obstructive megaureter), RALUR-EV (robot-assisted laparoscopic extravesical ureteral reimplantation), VCUG (voiding cystourethrography), VUJ (vesico-ureteric junction), UPJO (ureteropelvic junction obstruction), UTI (urinary tract infection), VUR (vesicoureteral reflux)

      1. Introduction

      In infants with primary obstructive megaureter (POM), conservative management is the first line of treatment. However, in those with uncontrollable urinary tract infections (UTIs) or high grade or progressive obstruction, ureteral reimplantation is indicated. Although the open approach of ureteral reimplantation is still regarded as the gold standard, laparoscopic and robot-assisted laparoscopic approach become rapidly adopted by pediatric urologists, and the minimally invasive surgery achieved the comparable success rates ranging from 72% to 99% [
      • Grimsby Gwen M.
      • et al.
      Multi-institutional review of outcomes of robot-assisted laparoscopic extravesical ureteral reimplantation.
      ,
      • Casale P.
      • Patel R.P.
      • Kolon T.F.
      Nerve sparing robotic extravesical ureteral reimplantation.
      ,
      • Kasturi S.
      • et al.
      Prospective long-term analysis of nerve-sparing extravesical robotic-assisted laparoscopic ureteral reimplantation.
      ,
      • Akhavan A.
      • Avery D.
      • Lendvay T.S.
      Robot-assisted extravesical ureteral reimplantation: outcomes and conclusions from 78 ureters.
      ,
      • Dangle P.P.
      • Shah A.
      • Gundeti M.S.
      Robot-assisted laparoscopic ureteric reimplantation: extravesical technique.
      ,
      • Herz D.
      • et al.
      Robot-assisted laparoscopic extravesical ureteral reimplant: a critical look at surgical outcomes.
      ,
      • Arlen A.M.
      • et al.
      Outcomes of complex robot-assisted extravesical ureteral reimplantation in the pediatric population.
      ] and less surgical trauma.
      It remains controversial if robot-assisted laparoscopic extravesical ureteral reimplantation (RALUR-EV) is suitable for infants with POM [
      • Farrugia M.K.
      • Hitchcock R.
      • Radford A.
      • et al.
      ]. In principle, to guarantee the successful establishment of anti reflux mechanism, the length of detrusor tunnel must be at least 5 times longer than the ureter's diameter [
      • PAQUIN Jr., AJ
      Ureterovesical anastomosis: the description and evaluation of a technique.
      ]. However, because the small infantile bladder limits the detrusor tunnel's length, many pediatric urologists argue that the operation is challenging [
      • Farrugia M.K.
      • Hitchcock R.
      • Radford A.
      • et al.
      ]. To ensure RALUR-EV can be carried out in infants with adequate tunnel/diameter ratio, we modified the technique. In this paper, we report our initial experience of RALUR-EV in a cohort of infants with primary obstructive megaureter (POM).

      2. Material and methods

      We retrospectively analyzed the clinical information of sixteen infants with POM who underwent RALUR-EV in our center from April 2017 to July 2019. Twelve of these patients had undergone endoscopic double-J stenting and endoscopic balloon dilatation alternately, combined with antibiotic therapy, these treatments had failed to control recurrent UTIs. For three patients, the guidewire of double-j stent couldn't pass through ureteral inlet by cystoscope. One two-month-old infant had undergone cutaneous nephrostomy, but the nephrostomy tube slipped out after two months. Based on the common ground that the guardians of these infants couldn't accept the nursing difficulties of cutaneous nephrostomy, to prevent the further renal function damage, the surgeon executed ureteral reimplantation on these infants. All operations employed the daVinci robotic Si surgical platform® (Intuitive Surgical, Sunnyvale, CA). There were 11 boys and 5 girls with a mean age of 7.4 ± 3.2 months. The patients were diagnosed as POM based on clinical symptoms, physical examination, abdominal ultrasonography, VCUG (voiding cystourethrogram), magnetic resonance urography or anterograde pyelogram, urodynamic study and/or diuretic renal dynamic imaging. Patients’ demographic data and perioperative clinical infromation are shown in Table 1. Indications for surgery of POM included ipsilateral function <40% at diagnosis or dropping below 40% during surveillance, recurrent UTIs , severe hydroureteronephrosis, or progression in hydroureteronephrosis. The surgical indications are consistent with the BAPU guidelines [
      • Farrugia M.K.
      • Hitchcock R.
      • Radford A.
      • et al.
      ]. The preoperative mean diameter of the megaureter was 1.7 ± 0.5 cm. Criteria for a successful operation was defined as relief of clinical symptoms, reduced dilation from preoperative measures and no high grade (III–V) reflux detected on postoperative VCUG. Patients with complex anatomy including bladder diverticula and posterior urethral valve were excluded from this study.
      Table 1Perioperative data of POM infants.
      ParameterValues
      Sex (n)
      Male11
      Female5
      Age, mo, mean (range); SD7.4 (4–12);3.2
      Side (n)
      Left8
      Right6
      Bilateral2
      Preoperative symptoms (n)
      UTI10
      None6
      Detected antenatally14
      Preoperative distal ureteric diameter,

      cm,mean (range); SD
      1.7 (1.2–2.8);0.5
      Preoperative split renal function,%, mean±SD43.6 ± 4.8
      UTI: urinary tract infection.

      2.1 Operative techniques

      The patients were placed in a 30° Trendelenburg position and secured with tape to the table. A Foley catheter was inserted the sterile for bladder instillation intra-operatively. An 8.5 mm camera port (C) was placed at the level of the umbilicus (in younger children with pubo-umbilical distance shorter than 6.0 cm, this was placed in a supra-umbilical postion). After establishing pneumopteritoneum, two 5 mm robotic trocars (R1, R2) and a 5 mm assistant port (A) were placed under direct camera vision, on each side of the camera port (4–6 cm), and in the right upper abdominal quadrant, respectively (Fig. 1).
      The ureter is identified at the pelvic brim. The peritoneum over the ureter is then incised and the ureter is mobilized to the level of the vas deferens or uterine artery. A peritoneal window is created distal to the vas deferens or uterine artery, and the ureter is freed underneath. The dissection is kept close to the ureter, especially at the vesico-ureteric junction (VUJ) and distal ureter, to preserve the presumed neurovascular bundle located dorsomedially [
      • Leissner J
      • Allhoff EP
      • Wolff W
      • et al.
      The pelvic plexus and antireflux surgery: topographical findings and clinical consequences.
      ]. The ureter is transected at the level of bladder mucosa and the narrowed ureteral segment is resected. Distal ureteral tailoring is performed if the megaureter is massively dilated (diameter>15 mm). We prefer to conduct extracorporeal ureteral tailoring. The megaureter is extracted through a robotic trocar incision on same side with the help of a laparoscopic grasper. (Fig. 2). After trimming the ureter, a feeding tube or ureteric catheter (10F) is then inserted into the ureter. The ureter is then tailored with continuous fashion with a 6–0 absorbable suture. The new ureterovesical junction is moved up 1 cm to preserve the pelvic complex.
      Fig 2
      Fig. 2A Double-J stent is inserted in the ureter before completion (a); The megaureter is extracted through the same side robotic trocar with a laparoscopic grasper and the trocar is temporarily removed, the megaureter is tapered under direct vision (b).
      The ureteroneocystostomy is conducted using 6–0 absorbable suture, and a Double-J stent is inserted in the ureter before completion (Fig. 2a).
      The bladder is then filled with saline (60 ml for more than 6 months, 50 ml for less than 6 months) to maintain a constant bladder distension. The detrusorotomy length and width are measured with premarked 4–0 silk. The median umbilical ligament is transected firstly, and part of anterior bladder wall is mobilised (Fig. 3). Then the detrusor tunnel is extended from vesicoureteral junction to anterior bladder wall. If the infantile posterior bladder wall is large enough to accommodate detrusor tunnel, the median umbilical ligament is also transected after the closure of detrusorotomy, to minimize angulation of ureter (Fig. 4). A transabdominal stay stitch across the anterior bladder wall is used to elevate the bladder and improve visualization during the closure of detrusorotomy.
      Fig 3
      Fig. 3The median umbilical ligament is transected, and the bladder is pulled down, then the entire detrusor tunnel is created from posterior bladder wall to anterior bladder wall. (a-bladder; b-reimplanted ureter; c-median umbilical ligament; d-premeasured detrusor tunnel).
      Fig 4
      Fig. 4The median umbilical ligament is transected after the closure of detrusorotomy, then the bladder is pulled down. (a-bladder; b-reimplanted ureter; c-median umbilical ligament; e- detrusor tunnel).
      The detrusorraphy is performed using a running stitch (5–0 PDS) using a bottom-up approach with incorporation of the ureteral adventitia. A stitch (5–0 PDS) is placed at the apex of the detrusorotomy through the ureteral adventitia to align the ureter within the tunnel [
      • Gundeti Mohan S.
      • Boysen William R.
      • Anup Shah
      Robot-assisted laparoscopic extravesical ureteral reimplantation: technique modifications contribute to optimized outcomes.
      ]. The bladder wall close to the reimplanted vesicoureteral junction is fixed onto the serosa of vas deferens (Fig. 5a) or the adjacent psoas (Fig. 5b) with 4–0 absorbable sutures. A drainage tube is inserted through the 8.5 mm port.
      The urinary catheter is removed on postoperative day 3 or 4 days. The drainage tube is removed 2–3 days after surgery. The Double-J stent is removed after 6 weeks. Postoperative complications are analyzed using the Clavien-Dindo classification [
      • Dindo D.
      • Demartines N.
      • Clavien P.A.
      Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.
      ]. All data are presented as mean ± standard deviation or medians with the ranges.

      2.2 Follow-up and statistical analysis

      Follow-up renal ultrasonography was performed 1, 3, 6 and 12 months post operatively, VCUG and postoperative diuretic renal dynamic imaging were obtained 6 month post operatively. Paired-Samples t-test was performed to evaluate statistical differences. Values of p < 0.05 were considered significant, and reported p values were two-sided.

      3. Results

      The patients’ postoperative results are shown in Table 2. Two patients were diagnosed with ipsilateral ureteropelvic junction obstruction (UPJO) and underwent pyeloplasty before reimplantation. All robotic surgeries were completed without conversion. Bilateral and unilateral reimplantation were performed in two and fourteen patients, respectively. Four ureters were tapered and then sutured to the bladder without any tension, all the tapered strictured segment were less than 1 cm. The mean operative time was 115.0 ± 19.5 min and the mean blood loss was 10.0 ± 1.8 ml. No intraoperative complication was observed. No postoperative urinary retention was observed. The mean postoperative stay was 4.5 ± 1.0 days. Among 16 patients treated for POM, hydroureteronephrosis improved in 15 patients, the mean distal ureteric diameter was significantly decreased from 1.7 ± 0.5 cm to 0.6 ± 0.5 cm 6 months post operatively (p < 0.05), and no statistically difference was found between preoperative and postoperative mean split renal function (43.6 ± 4.8% vs 42.9 ± 4.3%). The overall operative success rate was 94.4% (17 of 18 ureters) with a mean follow-up of 15.9 ± 7.4 months. One patient underwent balloon dilation and double-J stent insertion for postoperative vesicoureteric junction (VUJ) stenosis, further postoperative VCUG and ultrasonography at 6 months later showed no stenosis, and the postoperative diuretic renal dynamic showed the ipsilateral function was 42.8% (preoperative diuretic renal dynamic was 44.6%), this patient was managed with long-term outpatient follow-up and classified as Clavien-Dindo III. One patient had grade Ⅰ VUR and one had grade Ⅱ VUR on VCUG at 6 months postoperative. Two refluxing patients had recurrent UTIs postoperatively, who were managed with oral antibiotics successfully during the follow-up period. They were categorized as Clavien grade II complications (we suspect them to be stent complication).
      Table 2Postoperative profile of POM Patients.
      ParameterValues
      Tapering ureter reimplantation4
      Operative time, min, mean (range); SD115.0 (89–165); 19.5
      Estimated blood loss, mL, mean (range); SD10.0 (5–15); 1.8
      Postoperative hospital stay, d, mean (range); SD4.5 (3–7); 1.0
      Follow-up time, mo, mean (range); SD15.9 (7–31); 7.4
      Postoperative complication
      VUR (grade I)1
      VUR (grade II)1
      Obstruction1
      Postoperative distal ureteric diameter, cm, mean (range); SD0.6(0–1.9);0.5
      Postoperative split renal function,%, mean±SD42.9 ± 4.3
      VUR: vesicoureteric reflux.

      4. Discussion

      Nowadays, the treatment of infants with POM is still controversial, majority of pediatric urologists are prone to conservative management or temporary options, such as temporary double-J stenting, endoscopic balloon dilatation, endoureterotomy, cutaneous ureterostomy. These choices are not free from complications like urinary infections, stent migration, stenosis, lithiasis and so on [
      • MacGregor PS
      • Kay R
      • Straffon RA
      Cutaneous ureterostomy in children--long-term followup.
      ,
      • Giovanni T.
      • Agnese R.
      • Elisa B.
      • Francesco T.
      • Antonio F.
      • Di Iorio G.
      High-pressure balloon dilatation for the treatment of primary obstructive megaureter: is it the first line of treatment in children and infants?.
      ]. Although ureteral reimplantation with or without tempering is the ultimate management, it is still the gray zone in infants currently.
      These infants included in our center had received antibiotic prophylaxis, endoscopic double-J stenting, endoscopic balloon dilatation and cutaneous nephrostomy before they received ureteral reimplantation (Fig. 6) . Children may not benefit from long-term antibiotics prophylaxis, the unreasonable use of abtibiotics can generate antibiotic resistance, bone marrow repression, gastrointestinal side effects and severe drug reactions [

      Elder JS, Peters CA, Arant BS Jr, et al. Pediatric Vesicoureteral Reflux Guidelines Panel summary report on the management of primary vesicoureteral reflux in children. J Urol. 1997;157(5):1846-1851.vesicoureteral reflux in children. 1997, 157(5):1846–51.

      ]. Antibiotic prophylaxis cannot control infants’ febrile urinary tract infections in this study, so we choose alternative temporary surgical interventions, such as endoscopic double-J stenting, endoscopic balloon dilatation and cutaneous nephrostomy. These therapies may temporarily relieve the urinary obstruction, but infants still suffering from renal function damage caused by UTIs, and the nursing difficulty company with cutaneous ureterostomy or nephrostomy still bothering patients’ guardians. Athough ureteral reimplantation in infants is full of controversy, reimplantation can relieve the clinical symptoms from the etiology.
      Fig 6
      Fig. 6This patient was 7 months old, suffering from deteriorating renal function. The image of MRU and 3-D Reconstruction showed severe left POM, the guidewire of double-j stent could not pass through ureteral inlet by cystoscope before he received ureteral reimplantation.
      Our experience of RALUR-EV with modified technique in infants has demonstrated that such minimally invasive approach is feasible and has reasonably good short-term outcomes. The key of the modification is to mobilize the anterior wall of the bladder to (i) ensure adequate detrusor tunnel length/ureteral diameter ratio, and (ii) to minimize acute angulation of the ureter (which also reduces tension on the ureter) in infants. We believe that this modification will both improve the outcome of Lich-Gregoir procedure by adhering to the principle stringently and reduces risk of obstruction from angulation.
      There are few reports about ureteral reimplantation in infants, especially in laparoscopy and robotic surgery [
      • Peters CA
      • Mandell J
      • Lebowitz RL
      • et al.
      Congenital obstructed megaureters in early infancy: diagnosis and treatment.
      ,
      • Greenfield SP
      • Griswold JJ
      • Wan J
      Ureteral reimplantation in infants.
      ,
      • Liu C
      • Chin T
      • Wei C
      Surgical treatment of vesicoureteral reflux in infants under 3 months of age.
      ,
      • Emily Jude
      • Aniruddh D.
      • Andrew B.
      • Japinder K.
      • Naeem S.
      • et al.
      Intravesical ureteric reimplantation for primary obstructed megaureter in infants under 1 year of age.
      ,
      • de Kort L.M.O.
      • Klijn A.J.
      • Uiterwaal C.S.P.M.
      • de Jong T.P.V.M.
      • et al.
      Ureteral reimplantation in infants and children: effect on bladder function.
      ]. According to the published articles, open Lich-Gregoir approach get the high risks of pelvic plex damage, hence surgeons are prone to open intravesical approaches. Still there are a few surgeons explored extravesical approach, in 2019, Villanueva et al. report “mini’ extravesical open reimplant with ‘mini’ tapering” technique, 9 infants underwent open unilateral “mini” extravesical reimplantation [
      • Greenfield SP
      • Griswold JJ
      • Wan J
      Ureteral reimplantation in infants.
      ,
      • Villanueva C.A.
      ‘Mini’ extravesical reimplant with ‘mini’ tapering for infants younger than 6 months.
      ,
      • Peters CA
      • Mandell J
      • Lebowitz RL
      • et al.
      Congenital obstructed megaureters in early infancy: diagnosis and treatment.
      ,
      • Liu C
      • Chin T
      • Wei C
      Surgical treatment of vesicoureteral reflux in infants under 3 months of age.
      ,
      • Emily J.
      • et al.
      Intravesical ureteric reimplantation for primary obstructed megaureter in infants under 1 year of age.
      ]. With the advent of minimal invasive age, as intravesical robotic approach is limited by inflant bladder space, Lich-Gregoir approach is more suitable for robot-assisted laparoscopic ureteral reimplantation [
      • Yeung C.K.
      Minimally Invasive Management for Vesicoureteral Reflux in Infants and Young Children.
      ].
      The previous study demonstrated that surgeons can preserve neural structures with proper understanding of pelvic plexus's anatomy. The new ureterovesical junction is moved up 1 cm from previous position. We also find that using scissors instead of energy devices to taper the ureters can decrease the risks of nerve damage. Based on these experiences, surgeons can preserve the pelvic plexus to the maximum under the robotic arm's precise operation and 3-dimensional visions [,
      • Leissner J
      • Allhoff EP
      • Wolff W
      • et al.
      The pelvic plexus and antireflux surgery: topographical findings and clinical consequences.
      ,
      • David S.
      • Kelly C.
      • Poppas D.P.
      Nerve sparing extravesical repair of bilateral vesicoureteral reflux: description of technique and evaluation of urinary retention.
      ]. In this study, postoperative urinary retention was not observed in all patients, proving that pelvic plexus preservation is feasible by robotic surgery approach.
      The critical step of ureteral reimplantation is creating adequte length of detrusor tunnel. According to the study published by Paquin in 1959, to guarantee the successful establishment of anti-reflux mechanism, the length of submucosal tunnel must be at least 5 times longer than ureteral diameter [
      • PAQUIN Jr., AJ
      Ureterovesical anastomosis: the description and evaluation of a technique.
      ]. Most infants’ posterior bladder wall is large enough to create ureteral tunnel, but because the reimplanted vesicoureteral junction is relatively too high, ureteral angulation cannot be avoided after the ureteral reimplantation (Fig. 7A), so the purpose of procedures like transecting the median umbilical ligament, disassociating the anterior bladder wall is to decrease the ureteral angulation (Fig. 7B). In addition, another situation is that the infantile posterior bladder wall restricts the length of premeasured tunnel. To overcome this defect, these procedures like transecting the median umbilical ligament, disassociating the anterior bladder wall adhesion make it feasible that the premeasured detrusor tunnel can extend from vesicoureteral junction to the anterior bladder wall (Fig. 3).
      Fig 7
      Fig. 7A-The acute angle is formed by reimplanted ureter and posterior bladder wall, and this acute angle causes the potential risk of ureteral angulation. B-The transection of median umbilical ligament and the dissection of anterior bladder wall make it possible to relieve the ureteral angulation. The next fixation step of bladder can maintain this status to avoid the ureteral angulation recur.
      During the closure of detrusor tunnel, we applied the LUAA technique, including the use of a U stitch at the UVJ, incorporation of the adventitia into the alignment stitch and placement of an alignment stitch at the apex of the detrusor tunnel to minimize the possibility of ureteral slippage [
      • Kojima Y
      • Mizuno K
      • Umemoto Y
      • Yasui T
      • Hayashi Y
      • Kohri K
      Ureteral advancement in patients undergoing laparoscopic extravesical ureteral reimplantation for treatment of vesicoureteral reflux.
      ].
      During the bladder distension, we discovered that the bladder dome elevates and will adhere to the raw anterior abdominal wall, which generates ureteral angulation much more probably. To overcome anterior bladder wall's inertia of elevation, the bladder wall near the vesicoureteral junction is fixed on the adjacent psoas or the serosa of vas deferens. The choice of fixation site should be flexible, if the serosa of vas deferens is too thin to overcome this inertia or the bladder after dissociated is of high mobility, psoas fixation will be the better site (Fig. 8A,B). According to the observation of intraoperative bladder saline perfusion, ureteral angulation didn't accur on any patients after bladder fixation, and all patients voided smoothly during the follow-up period (Including the patient after the second operation).
      Fig 8
      Fig. 8A-the bladder wall near the reimplanted vesicoureteral junction is fixed on the adjacent serosa of vas deferens or round ligament of uterus; B-Adjacent psoas is the alternative fixation site.
      In this study, 16 patients (18 ureters) underwent our procedure, all of the patients (including 2 bilateral cases) were symptomatically recovered, no postoperative voiding dysfunction was reported with a mean follow-up of 15.9 months, the high success rate demonstrates its feasibility and safety for the treatment of POM, and further, for the treatment of infantile ureteral reimplantation. Considering low-grade vesicoureteral reflux get nearly 80% resolution rate in grade I and II reflux [
      • Elder J.S.
      • Peters C.A.
      • Arant B.S.
      • et al.
      Pediatric vesicoureteral reflux guidelines panel summary report on the management of primary vesicoureteral reflux in children.
      ], and two refluxing infants’ postoperative UTIs can be controlled conservatively, we defined postoperative low-grade reflux as one of successful operation criteria in this study.
      We initially applied this modified technique on the treatment of POM infants, and proposed hypothesis that the technique can be applied on infants with congenital abnormalities of the ureterovesical junction, whose ureters needed to be reimplanted, such as infantile VUR, duplex system ureterocele that transurethral fenestration cannot alleviate the symptoms. We will test the hypothesis clinically in the future.
      Limitations of the current study is its retrospective nature, lack of control group, a relatively small number of this cohort and the relatively short follow-up period restricting further conclusion. A prospective multi-center study is indispensable to prove the safety and feasibility of this technique.

      Ethical approval

      The study was approved by the Ethics Review Board of the Seventh Medical center of Chinese PLA General Hospital (registration number: 2013-078).

      Acknowledgments

      This work is supported by the Military Family Planning Fund [ 18JS001 ], Beijing Municipal Science and Technology Plan [No. Z181100001718008 ], National Public Welfare Industry Research Projects [No. 201402007 ], Capital Health Development Research Fund [No. 2016-2-5091 ].

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