{"paper_id":"eee4a08b-add0-45b8-bd73-1202194b5356","body_text":"VU Research Portal\nUreteral injuries during Laparoscopic Hysterectomy\nJanssen, P.F.\n2013\ndocument version\nPublisher's PDF, also known as Version of record\nLink to publication in VU Research Portal\ncitation for published version (APA)\nJanssen, P. F. (2013). Ureteral injuries during Laparoscopic Hysterectomy. [, Vrije Universiteit Amsterdam].\nGeneral rights\nCopyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners\nand it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights.\n            • Users may download and print one copy of any publication from the public portal for the purpose of private study or research.\n            • You may not further distribute the material or use it for any profit-making activity or commercial gain\n            • You may freely distribute the URL identifying the publication in the public portal\nTake down policy\nIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately\nand investigate your claim.\nE-mail address:\nvuresearchportal.ub@vu.nl\nDownload date: 27. Jun. 2026\n\n7\nP .F. Janssen\nH.A.M. Brölmann\nJ.A.F. Huirne\nSurg Endosc. 2013 Mar; 27(3): 946-956\nCAUSES AND PREVENTION  \nOF LAPAROSCOPIC URETER INJURIES: \nAN ANALYSIS OF 31 CASES DURING \nLAPAROSCOPIC HYSTERECTOMY  \nIN THE NETHERLANDS\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nABSTRACT\nBackground\nUreter injuries are the most dreaded complication in gynaecological surgery. Some risk \nfactors for the occurrence of urinary tract injuries are known, but clear guidelines to prevent \nureter injuries during laparoscopic hysterectomy (LH) are lacking. The aim of this study was \nto analyze all known ureter injuries that occurred during LH for a benign indication, in the \nNetherlands, in order to identify patient- and surgeon-related risk factors.\nMethods\nNinety-five LH-performing gynecologists were asked to recall all cases of known ureter \ninjuries during LH in their hospital. After identification of ureter injuries, a structured \ninterview was performed with a questionnaire that focused on the identification of \npredisposing factors which could account for the cause of the injury.\nResults\nForty-one injuries were detected in 37 patients (4 bilateral ureter injuries) in a 20-year \nperiod. The questionnaire could be completed for 31 cases. Predisposing factors \nwere retrospectively assessed and classified into categories: patient-related (i.e., \ndeep infiltrating endometriosis, intraligamentary fibroids) (n=18), surgeon-related \n(insufficient experience and/or technique) (n=16), or both (insufficient experience and \ndifficult case) (n=8). According to earlier-mentioned recommendations in a Delphi \nstudy among experts, in 48.4% of these ureter injury cases more than one of the \nrecommended techniques or predisposing conditions were not applied or available. \nOnly one ureter injury was diagnosed during the LH; the mean time to diagnose the \ninjury was 29 days.\nConclusions\nIncomplete learning curve, insufficient applied technique such as coagulation of the \nuterine artery without the use of an uterine manipulator and/or from the contralateral \nside and/or without previously performed ureterolysis in case of distorted anatomy \nmay be considered as the main predisposing factors.\n106\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nINTRODUCTION\nUreter injuries are the most dreaded complication in gynaecological surgery. The \ncourse of the ureter in the pelvis renders it liable to injury during gynaecological \noperations, particularly during hysterectomies 1. The reported incidence of ureter \ninjuries during hysterectomies varies between 0 and 2.2% 2-7. The approach of the \nhysterectomy plays a role in this variation of incidence. A systematic review, including \n29 randomized controlled trials (RCTs) comparing the laparoscopic with the abdominal \nand vaginal approaches, reported an Odds Ratio (OR) of 2.41 (95% CI: 1.21 - 4.82) \nfor urinary tract injuries in the laparoscopic group compared to the abdominal group \nand an OR of 3.69 (95% CI: 1.11 - 12.24) comparing total laparoscopic hysterectomy \n(LH) with the vaginal approach 8. A learning curve with respect to urinary tract injuries \nhas been reported. The risk of a ureter injury significantly decreased with increasing \nexperience of the surgeon with a cutoff level of 30 performed LHs 5. The role of a \nlearning curve has also been postulated in 2001 after the analyses of a large Finnish \ndatabase, including all 10.110 hysterectomies performed because of a benign \nindication in 1996. The incidence of ureter injury decreased significantly from 2.2 to \n0.5% when the surgeons had performed more than 30 LHs compared to those who \nperformed 30 or fewer LHs 3. Ten years later, a substantially lower incidence of ureter \ninjuries was reported during LH in the same database, which resembled the reported \nincidence during abdominal (0.3%) and vaginal hysterectomy (0.04%) 9. Nevertheless, \nureter injuries also occur in the hands of experienced gynecologists, as the indication \nfor LH is expanding and the difficulty of the operation is increasing 10. \nSome risk factors for the occurrence of urinary tract injuries are known, such as the \npresence of deep infiltrating endometriosis, dense adhesions, very large uteri and \nexcessive bleeding 5. However, clear guidelines for indications, surgical experience, \nor surgical techniques to prevent ureter injuries during LH are lacking. Based on a \nrecent consensus-based Delphi procedure (which is a method to achieve consensus \nin dealing with a complex problem by structuring a group communication process) \namong laparoscopic experts, several recommendations were formulated 11. \nGiven the low incidence of ureter injuries, much can be learned from each \nindividual case. In order to increase our knowledge, we performed a systematic search \nto identify and analyze all known ureter injuries that occurred during LH in the first \ntwenty years after the introduction of this procedure in the Netherlands. The aim of \nthis study was to identify patient- and surgeon-related risk factors for ureteral injuries \nduring a laparoscopic hysterectomy.\nMATERIAL AND METHODS\nCase selection\nWe retrospectively analyzed all recalled ureter injuries that occurred in the Netherlands \nfrom 1991 to 2011 during a LH of all types: total laparoscopic hysterectomy (TLH), \nlaparoscopic-assisted vaginal hysterectomy (LAVH), and laparoscopic supracervical \n107\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nhysterectomy (LSH). In an attempt to identify all known ureter injuries during these \nprocedures, we systematically contacted all gynecological departments in April 2009 in \nthe Netherlands and asked for the names of all gynaecologists who performed or currently \nperform LHs. We contacted all LH-performing gynaecologists (n=95) by both mail and \ntelephone and asked them to recall all cases of known ureter injuries during LH in their \nor any other hospital. In addition, we studied all available annual reports of the hospitals \nin the Netherlands from 2000 onward in order to identify additional ureter injuries. We \ncontacted all LH-performing gynecologists again in 2011 and asked them to report all \nadditional identified ureter injuries (Figure 1). All identified cases of ureter injuries were \nstudied and responsible surgeons or first assistants were contacted for a structured \ninterview using a questionnaire that focused on identifying predisposing factors that could \naccount for the cause of the injury. All known cases were studied, surgical reports were \nreviewed for their various procedural steps, and recorded videos were studied if available.   \nLH‐performing hospitals \nn=64 \nLH‐performing gynaecologists \nn=95\nUreter injuries \nidentified \nn=26 \n100 hospitals \nin the \nNetherlands \nAdditional \nureter injuries \ndiagnosed \nn=11\nUreter injury cases \nidentified \nn=37 \nUreter injury cases \nanalyzed \nn=31 \nCases not analyzed \nn=6 \n‐ 4 lack of participation \n‐2 lack of information \n2nd round \ninterrogation \nof hospitals \nand surgeons  \n(January 2011) \nInterrogation \nof hospitals \nand surgeons \n(April 2009) \nIdentification Enrolment Analysis \nFigure 1. Flowchart for identifying ureter injury cases\n108\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nDevelopment of the questionnaire used during interviews\nThe development of the questionnaire was based on a systematic literature search \nand a Delphi consensus procedure among gynecological laparoscopic experts in the \nfield of LH 11. Most predominant consented factors and formulated recommendations \nto prevent ureter injuries during LH and to prevent a delay in its diagnosis were \nintegrated in our questionnaire. These factors could be (1) patient-related (i.e., \nindication for surgery, size of the uterus, presence of intraligamentary fibroids, deep \ninfiltrating endometriosis, dense adhesions, previous abdominal surgery and other \ncomorbidity); (2) surgeon-related (i.e., surgical team, learning curve, annual case \nload); (3) procedure-related (i.e., equipment and protocols used, level of identification \nor dissection of the ureter); and (4) diagnostic process during or after surgery in \norder to identify or exclude a ureter injury. We asked all surgeons what they thought \nwas the main predisposing factor and their subjective observation and beliefs about \nthe cause of the ureter injury in their particular case. We asked them if this ureter \ninjury case changed their common practice with respect to patient selection, applied \ntechnique, or instruments used.\nData collection and Analysis\nIn order to identify the most common predisposing and potential causative factors of \nureter injuries, we critically studied all cases; recorded baseline characteristics, applied \ntechniques, and instruments used; and recorded presentation and timing of related \nsymptoms, applied diagnostic methods, and findings during ureter reconstruction \nor performed therapy, its side, and location. We compared potential predisposing \nfactors in each individual case with the previous agreed upon recommendations 11. \nAll results were analyzed using the SPSS® version 16.0 statistical software package \n(SPSS Inc., Chicago, IL, USA).\nRESULTS\nNumber of injuries\nThe laparoscopic hysterectomy was first performed in the Netherlands in 1991. Of \nthe 100 hospitals in the Netherlands, 64 performed LHs over time. After the initial \nround of interrogating the LH-performing gynecologists, 26 ureter injury cases were \nidentified (Figure 1). The survey was repeated in 2011 and 11 additional cases of \nureter injuries were identified, resulting in a total of 41 injuries in 37 patients (four \nwomen had bilateral ureter injuries). The reported injuries occurred between April \n1994 and November 2010. The cases were identified in 25 different hospitals: 3 \nuniversity hospitals, 12 general teaching hospitals, and 10 nonteaching hospitals. The \nquestionnaire could be completed in 31 cases. Of the other six cases, the available \ndata were insufficient to complete the questionnaire. In these cases only some of the \nquestions could be answered (Figure 1).\n109\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nTable 1. Baseline patient characteristics\nTLH\n(N=22)\nLAVH\n(N=6)\nLSH\n(N=3)\nTotal\n(N=31)\nAge (mean ± SD) (years) 45.3 46.0 43.7 45.3 ± 7.1\nBMI (mean ± SD) (kg/m 2) 27.0 27.8 - 27.1 ± 4.4\nParity (mean) 2.0 1.6 2.7 2.0 ± 1.17\n≥ 1 caesarean section [n(%)] 4 0 1 5 (16)\nPrior abdominal surgery a [n(%)] 9 2 0 11 (35.5)\nIndication for hysterectomy [n(%)]\nAbnormal bleeding 13 3 3 19 (61.3)\nPelvic pain 4 2 0 6 (19.4)\nOther 5 1 0 6 (19.4)\nFibroids [n(%)] 14 3 3 20 (64.5)\na Other than caesarean section\nPatient baseline characteristics\nIn the identified cases with ureter injuries, the main registered indication for performing \nLH was an uterine bleeding disorder (Table 1). Body mass index (BMI) ranged from \n21.5 to 39.0, with a mean of 27.1 (SD 4.4). Previous abdominal surgery (other than \ncaesarean section) was present in 11 patients (35.5%). In four cases (12.9%), deep \ninfiltrating endometriosis was observed. Uterine fibroids were present in 20 of the 31 \ncases (64.5%); one had a large fibroid with an intraligamentary location. The uterine \nweight ranged from 60 to 896 g (mean = 271.4 g, SD = 211.2), and in 11 cases (35.5%) \nit was >250  g. Dense adhesions were present in seven patients (22.6%).\nSurgeon-related factors\nThe total number of previous performed LHs by the first surgeon before the injury \noccurred ranged between 2 and 300, with a mean of 69.5 (SD = 78.0). The annual \ncase-load of LHs ranged from 5 to 75, with a mean of 19.4 (SD = 13.9). In 18 cases \n(58.1%), the primary surgeon had performed fewer than 60 previous LHs, and in 11 \ncases (35.5%) fewer than 30 LHs. In eight cases (25.8%), the experience of the surgical \nteam was fewer than 30 LHs, i.e., the first surgeon and the primary assistant had both \nperformed fewer than 30 LHs before the particular ureter injury case occurred.\nOperative procedure\nEquipment\nA uterine manipulator had been used in 26 cases (83.9%), and in the majority of the cases \nit was a Clermont Ferrand manipulator (54.8%) (Table 2). In two cases no manipulator \nwas used and in three cases the surgical report was unclear and the item could not \nbe recalled by the surgeon. In general, three or more trocars were placed (90.3%). In \none case only one additional trocar was used besides the optical trocar. Single port \n110\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nwas not used in these cases. Modalities used to achieve hemostasis of the uterine \nvessels during LH were conventional bipolar coagulation, vessel sealing, and ultrasonic \ntechnique (Table 2). In case of a bleeding (n = 9), the most common instrument used to \nachieve hemostasis was a conventional bipolar coagulating instrument.\nProcedure and surgical outcome\nProcedural aspects and surgical outcome in terms of operating time and blood loss \nare reported in Table 2. Of the 31 cases, there were 22 TLHs, 6 LAVHs, and 3 LSHs. In \neight cases, a concomitant salpingo-oophorectomy (uni- or bilateral) was performed \nTable 2. Operative proc edure\nTLH\n(N=22)\nLAVH\n(N=6)\nLSH\n(N=3)\nTotal\n(N=31)\nEquipment\nUterine manipulator [n(%)]\nClermont Ferrand 12 2 3 17 (54.8)\nMcCartney tube 2 0 0 2 (6.5)\nOther with vaginal   shield a 3 0 0 3 (9.7)\nOther without vaginal shield b 1 3 0 4 (12.9)\nUnknown 2 1 0 3 (9.7)\nNone 2 0 0 2 (6.5)\nHaemostatic instrument [n(%)]\nVessel sealing 13 2 0 15 (48.4)\nUltrasonic 1 2 0 3 (9.7)\nConventional bipolar 6 1 3 10 (38.7)\nUnknown 2 1 0 3 (9.7)\nProcedure\nConcomitant salpingo-oophorectomy [n(%)] 7 1 0 8 (25.8)\nUreter handling\nVisualization ureter [n(%)] 6 1 2 9 (29.0)\nWindow in broad ligament [n(%)] 7 0 0 7 (22.6)\nLateralizing ureter [n(%)] 6 1 0 7 (22.6)\nDissection ureter [n(%)] 1 0 0 1 (3.2)\nVaginal closure vaginal cuff [n(%)] 6 5 - 11 (35.5)\nOutcome\nBlood loss (mean ± SD) (mL) 184.3 425.0 316.7 245.7 ± 288.4\nOperating time (mean ± SD) (min) 137.0 149.8 174.3 143.5 ± 53.8\nTLH total laparoscopic hysterectomy, LAVH laparoscopic-assisted vaginal hysterectomy, LSH laparoscopic \nsupracervical hysterectomy\n a Pelosi, Colpo probe, Hohl-manipulator\nb V-care\n111\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\n(Table 2). The uterine arteries were coagulated from the ipsilateral side in 17 cases, \nfrom the contralateral side in 7 cases, and the surgeon could not recall the applied \ndirection in 7 cases.\nWe asked all surgeons whether or which perioperative measures were taken to \nidentify or dissect the ureter (Table 2B). Preventive placement of ureter stents pre- or \nintraoperatively was not done.\nDiagnosis\nUreter injury was identified between 0 and 260 days after surgery; one ureter injury was \nidentified during primary surgery and in four cases within 1 week after the operation. Most \ncases (90.3%) were identified within 1 month after primary surgery, with a mean delay of \n29 days (SD = 54) (Table 3). In 67.7% (21/31) of the cases, the ureter injury was located on \nthe right side and in four cases it was bilateral. Most of the injuries (87.1%) were located \nat the distal third part of the ureter (Figure 2). The only patient with a proximal location of \nthe ureter injury had an uterus of 896 g with a large intraligamentary fibroid.\nIn one case an intravenous excretory urography was performed during the primary \nsurgery because of a suspected ureter injury possibly resulting from difficult hemostasis. \nThe urologist had already been consulted because of a bladder injury during the same \nprocedure. Since stenting the ureter at the right side during cystoscopy failed, he decided \nto perform ureterolysis using an open approach, followed by a neo-implantation of the \nureter in the bladder because of a detected injury. In the other 30 cases no diagnostic \nmethods were applied during primary surgery. In one case a Doppler ultrasound of the \nbladder was performed in the postoperative admission period. Due to a double ureter \nat the injured side, ureteral flow was observed at both sides despite the injury.\nThe most common clinical signs and symptoms of ureter injury were abdominal \nand/or flank pain (58.1%), fever (16.1%), and urine leakage (12.9%). The most common \napplied diagnostic methods used to detect the injury were intravenous pyelogram \nTable 3. Time of recognition ureter injuries\nMoment of diagnosis [n(%)]\nTLH\n(N=22)\nLAVH\n(N=6)\nLSH\n(N=3)\nTotal\n(N=31)\nDuring primary operation 0 1 0 1 (3.2)\nDuring postoperative admission 0 0 0 0\nDuring re-admission 19 5 3 27 (87.1)\nPostoperative pain 11 4 3 18 (58.1)\nPostoperative fever 4 1 0 5 (16.1)\nPostoperative vaginal  leakage of urine 4 0 0 4 (12.9)\nUnknown 3 0 0 3 (9.7)\nTime until identification (mean ± SD) (days) 37.4 ± 63.7 10.2 ± 5.8 8.7 ± 4.0 29.0 ± 54.0\nTLH total laparoscopic hysterectomy, LAVH laparoscopic-assisted vaginal hysterectomy, LSH laparoscopic \nsupracervical hysterectomy\n112\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\n \n \n \n2 (including 1 \nbilateral) \n18 (including \n3 bilateral) \n0 \n2 (including 1 \nbilateral) \n12 (including \n3 bilateral) \n1 \nFigure 2. Localization and number of ureter injuries. The circled areas are the anatomical sites where the ureter \nis most likely to be injured during the laparoscopic hysterectomy (figure published in Baggish MH, Karam MM \n(2006) Surgical Anatomies of the bladder and ureter. In: Atlas of Pelvic Anatomy and Gynecologic Surgery. \nPhiladelphia: Saunders © Elsevier).\n(n = 8), computed tomography with contrast (n = 8), and (Doppler) ultrasound of the \nkidney and bladder to assess the ureteral flow (n = 7).\nTreatment and outcome\nAll ureter injuries were repaired by urologists, and ureter catheterization was carried \nout in 26 of the 35 ureter injuries. Successful retrograde stenting was performed for \n12 injured ureters. In 14 cases stenting was not possible via the retrograde route so \nan antegrade passage by means of a nephrostomy was used. Subsequent surgical \nrepair was carried out in 22 patients, all by an open procedure. The repair modalities \nused were (1) “spontaneous” recovery after ureter catheterization (n = 9), of which \none case per open surgery, (2) end-to-end anastomosis of the damaged ureter (n = 1), \nand (3) ureteroneocystostomy with or without psoas muscle hitch (n = 20). Immediate \nrepair was carried out in one case that was discovered during primary surgery after \n113\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nconverting the operation to open surgery. Ureter stents were left in place after surgical \nrepair in all cases and removed after a couple of weeks. As far as we know, all patients \nhad a successful repair with normal kidney function and no urine incontinence.\nPredisposing factors\nSubjective retrospective judgment of possible predisposing factors of the ureter injury \nin their own case by the surgeons\nIn ten cases (32.3%), an uneventful LH procedure was reported. Five surgeons \nreviewed the LH in retrospect as more difficult than expected. Nine surgeons rated \nthe procedure as difficult, with a score of more than 5 (on a scale of 0 to 10). Surgical \ndifficulties due to distorted anatomy were reported in eight cases (25.8%): dense \nadhesions (n = 7), deep infiltrating endometriosis (n = 4), and intraligamentary \nfibroids (n = 1). Heavy bleeding occurred in nine cases. Potential causal factors of the \nureter injury, as reported by the surgeons, were extensive coagulation in case of a \nbleeding (n = 5), coagulation too lateral (n = 14), lack of previous experience with LH \n(n = 1), dissection too distal and lateral (n = 1), and distortion of normal anatomy (i.e., \nendometriosis, dense adhesions, and large fibroids) (n=4). In six cases the surgeon \ncould not determine any possible predisposing factor.\nNine gynecologists changed their surgical technique after the case. Mentioned changes \nwere assistance from a more experienced gynaecologist during LH (n = 2), lateralization \nof the ureter during all LHs (n=2), routine use of an uterine manipulator (n = 1) or more \nthan two trocars (n = 1), coagulating the uterine pedicle closer to the uterus (n = 1), \nroutine visualization of the ureter at the end of the procedure, and in case of insufficient \nperistalsis of the ureter, performance of ultrasound of the bladder for the assessment of \nureteral flow on the first postoperative day (n = 1). In one case with severe deep infiltrating \nendometriosis, it became clear, after reviewing the recorded video, that after opening \nthe retroperitoneum and performing adhesiolysis at the pelvic side wall, the ureter was \ndislocated medially and firmly attached to the torus uteri (uterorectal space). Based on this \ncase the responsible gynecologists changed their protocol: complete ureterolysis before \nany other steps are taken in case of deep infiltrating endometriosis or dense adhesions.\nWe asked all gynecologists about their current policy with respect to ureter \nhandling during their LHs. Seven gynecologists stated that they dissected the ureter \nduring all LHs, 13 only if indicated (e.g., in case of distorted anatomy), and three \ngynaecologists stated “mostly not”.\nWe also asked all gynecologists about their diagnostic methods for excluding any \nureter injuries during routine LHs and in case of a suspected injury. Reported routine \ndiagnostic methods were intraoperative cystoscopy in all cases (n = 1), cystoscopy in \ncase of a suspected ureter injury (n = 4), and routine Doppler ultrasound of the bladder \nfor ureteral flow detection (n = 1). Reported protocols with respect to intraoperative \nprocedures in case of a suspected ureter injury included intravenous indigo carmine \nor methylene blue (n = 10), catheterization/stenting of the ureter (n = 7), visualization \nof the ureter (n = 3), and cystoscopy (n = 2).\n114\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nClassification of potential predisposing factors by the authors\nPotential predisposing factors were retrospectively assessed by two of the authors \n(PJ and JH) and classified according the earlier-mentioned groups: patient-related \n(n = 18), surgeon-related (n = 16), or a combination of both (n = 8).\nAssuming that the recommendations, recently agreed upon by the experts in the \nDelphi study, to be the standard of care and the agreed upon protocol that should be \nfollowed when performing a LH 11, we assessed to what extent these recommendations \nwere followed (Table 4). When a recommendation was not followed, we defined that \nas a “protocol violation”.\na. The learning curve was proposed to be completed by 20 LHs in case of normal \nanatomy and normal-sized uteri and 30 in case of large uteri 11. In case of severe en-\ndometriosis or intraligamentary fibroids consensus on number needed to complete \nthe learning curve was not reached, but it varied between 30 and >50 performed \nLHs. Thus, 11 cases (35.5%) may be considered as “protocol violations” with respect \nto the completed learning curve of the team, taking the anatomy into account.\nb. It was recently agreed upon that a uterine manipulator should always be used and \nthe uterine pedicle should be coagulated close to the uterus with a perpendicular \napproach 11. The latter can be achieved only if the uterine pedicle is coagulated \nfrom the ipsilateral side. Thus, at this point, eight cases (25.8%) may be considered \n“protocol violations”. \nc. Visualization or dissection of the ureter was recommended in case of distorted \nanatomy. According to this recommendation, in 9 of the 31 cases, the ureter should \nhave been identified; in seven of these nine cases the ureter was visualized and in one \ncase the ureter was dissected. Thus, one case may be considered a “protocol viola -\ntion” with respect to ureter visualization or dissection in case of distorted anatomy.\nIn 29 cases no standard intra- or postoperative cystoscopy or other diagnostic method \nwas applied. No diagnostic method was used in cases of reported dense adhesions or \ndeep infiltrating endometriosis (n = 7) or when a procedure was more difficult to perform \nthen expected by the surgeon (n = 5). In one of these cases, protracted recovery by \nthe patient, with the presence of abdominal pain and fever, was the reason to use \nadditional diagnostic methods (cystoscopy, computed tomography, and intravenous \nexcretory urography) on the fourth postoperative day. In the other cases the reported \npostoperative recovery period was judged to be uneventful during admission.\nDISCUSSION\nWe performed a systematic search to obtain nationwide data on iatrogenic ureter injuries \nduring laparoscopic hysterectomy for benign indications. To our knowledge this is the first \nindividual patient analysis of such a large number of ureter injuries during this procedure.\nIn more than one-third of the injury cases, the primary surgeon performed fewer \nthan 30 laparoscopic hysterectomies, and in one-fourth of the cases, the entire team had \nperformed fewer than 30 LHs. The learning curve for laparoscopic hysterectomy should be \n115\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nTable 4. Predisposing factors of ureter injury cases and “protocol violation” d\nCase Years Patient-related a Surgeon-related b\nPatient-a and \nsurgeon-\nbrelated\nUreter \ndissection\nUreter \nhandlingc\n“Protocol \nviolation”d\nLaparoscopic assisted vaginal hysterectomy (LAVH)\n1 1994 >12/395 g Team < 30 + - - +\n2 2006 >12/560 g - - -\n3 2006 <12/257 g - - -\n4e 2008 <12/95 g 1st < 30; contralat. - - +\n5 2009 <12 Team < 30 - - +\n6 2010 <12/104 g - + -\nTotal laparoscopic hysterectomy (TLH)\n7e 2003 >12/224 g - - -\n8e 2003 >12/490 g No manipulator + - - +\n9 2006 >18/415 g Team < 30; contralat. + - + +\n10 2006 896 g; intralig. fibroid Contralat. + - + +\n11 2007 <12/127 g; adh. - + -\n12 2007 <12/200 g Team < 30; contralat. - - +\n13 2007 <12 - - -\n14 2008 >12/130 g - - -\n15 2008 <12/90 g - - -\n16 2008 >12; DIE/adh. + + -\n17 2008 <12/120 g Team < 30 - - +\n18 2008 <12 Team < 30 - - +\n19 2008 <12 team<30 - - +\n20 2009 <12; DIE/adh. 1st < 30 + - - +\n21e 2009 <12/60 g + + -\n22 2010 <12/80 g Contralat.; no \nmanipulator - - +\n23 2010 >12/250 g - - -\n24 2010 <12/100 g; DIE/adh. Team < 30 + - + +\n25 2010 >12 - - -\n26 2010 >12/258 g + + -\n27 2010 <12; adh. Contralat. + + + +\n28 2010 <12/135 g 1st < 30 - + -\ncompleted by 20-30 procedures for a “simple” LH with normal anatomy and small-sized \nuteri 3, 11, and more than 30 LHs are needed to complete the learning curve for complicated \nLH (intraligamentary fibroids, dense adhesions, distorted anatomy). In 45% of the ureter \ninjury cases, the uteri were small (<12 weeks gestational age) and normal anatomy was \npresent without any adhesions or endometriosis. In these cases a failure of the applied \n116\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nTable 4. Continued\nCase Years Patient-related a Surgeon-related b\nPatient-a and \nsurgeon-\nbrelated\nUreter \ndissection\nUreter \nhandlingc\n“Protocol \nviolation”d\nLaparoscopic supracervical hysterectomy (LSH)\n29 2006 >12/376 g; adh. + + -\n30 2006 >12/618 g; DIE/adh. - + -\n31 2009 >12/262 g Contralat. + - - +\nTotal protocol violation [n(%)] 15 (48.4%)\ng uterine weight in grams, a dh. dense adhesions, DIE deep infiltrating endometriosis\na Patient-related is defined as uterine size over 12 weeks gestation, existence of deep infiltrating endometriosis, and/\nor dense adhesions and/or intraligamentary fibroids. Uterine size is expressed as size < 12 weeks, > 12 weeks, or > \n18 weeks of gestation (<12, >12 or > 18, respectively) and uterine weight in grams (g)\nb Surgeon-related is defined as the surgical team performed fewer than 30 previous LHs (<30 LHs) and/or the \nfirst surgeon performed fewer than 30 previous LHs ( 1 st < 30) and/or contralateral coagulation of the uterine \npedicle (contralat.) and/or procedure performed without the use of an uterus manipulator (no manipulator)\nc Ureter handling is  defined as ureter visualization and/or lateralizing of the ureter (e.g., making a window in \nthe broad ligament)\n d Protocol violation is defined as deviation of the previous recommendations as agreed upon by the expert \nteam in the Delphi procedure in order to prevent ureter injuries during laparoscopic hysterectomy 11\ne Ureter injury at both sides\ntechnique or insufficient knowledge of the anatomy and equipment may have played a \nrole. This suggestion is partly underlined by the fact that in more than half of the cases with \na normal anatomy, the primary surgeon had previously performed fewer than 30 LHs. This \nis also in line with the 50% ureter injuries that occurred without any predisposing factor and \nin 30% of the cases in uncomplicated small-sized uteri in the Finnish database 2.\nThe main difference between laparoscopic and total abdominal hysterectomy is the \nuse of electrocoagulation of uterine vessels during laparoscopic procedures 2. Excessive \nelectrocoagulation of uterine vessels and cardinal ligaments near the ureter increases the \nrisk of ureter injuries. In addition, the electrical current may damage the vascular supply \nand perivascular tissue, leading to delayed tissue necrosis and lateral thermal damage. It \nis difficult to estimate the exact number of ureter cases related to coagulating activities. \nHowever, given the subjective judgement of the surgeons about the cause of ureter \ninjuries, the delay in symptom presentation, and findings during ureter repair procedures, \nwe estimate electrocoagulation to be involved in more than half of our cases. There does \nnot seem to be a relationship with the type of instrument used for coagulation. Given \nthe lack of comparative studies on ureter injuries or complications as the end point, the \noptimal coagulating instrument to be used during laparoscopic hysterectomies can not \nbe defined. As proposed previously, the level of experience is probably more important in \npreventing urinary tract injuries than the type of instrument used 11.\nIdentification, dissection and lateralization of the ureter before securing the uterine \narteries are proposed by several authors to prevent ureter injuries 12-14. Although the \nureter may often be visualized through the peritoneum in the upper pelvis, it cannot \nbe identified reliably in the area of the cardinal ligaments. Particularly in the presence \n117\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nof distorted anatomy due to endometriosis or fibroids, the peritoneum is thickened and \nfibrosis retracts the ureter closer to the uterus 15. Lateralization of the ureter during the so-\ncalled “Koh manoeuvre”, which is supposed to prevent ureter injuries 12, is mostly difficult \nto achieve when there is of distorted anatomy, so ureterolysis is required in these cases to \nidentify and free the ureter. In a systematic Delphi procedure, it was not recommended \nthat ureterolysis should be performed on a routine basis but only in patients with \ndistorted anatomy near the uterine artery 11. Only one case (4%) of the known ureter injury \nlocations was located at the pelvic side wall. Furthermore, in seven cases the ureter was \nlateralized from the operating field. It is not clear if in all these cases the lateralization was \nperformed using the Koh manoeuvre. However, distortion of the anatomy was present in \nfive of these seven cases, complicating the performance of a successful Koh manoeuvre. \nThis shows that visualization of the ureter at the pelvic side wall is not sufficient and \nthat visualization or complete ureterolysis up to the uterine vessels should have been \nconsidered, particularly in case of distorted anatomy or large uteri.\nRecommendations for the applied technique in order to reduce the risk on \nurinary tract injuries were previously agreed upon by experts in a Delphi consensus \nprocedure 11. In comparison to the previously reported agreed upon recommendations, \nin 48.4% of the cases not all of these recommendations were followed. We called them \nprotocol violations. Strictly speaking, this is not the correct term to use since all cases \nwere performed before the recommendations were published and up to now there is \nno approved guideline on this subject in the Netherlands. In addition, it can not be \nproven that all ureter injuries would have been prevented if the recommendations had \nbeen followed in all cases. However, some of these recommendations, such as the use \nof an uterine manipulator, are easy to implement.\nTo prevent long-term complications such as urinoma or reduced kidney function, \nureter injuries should be recognized as soon as possible. An ureter injury is repaired more \neasily if discovered intraoperatively and patients would not need to be subjected to a \nsecond major unplanned extensive reoperation. In our study, the mean time to diagnose \na ureter complication was almost 1 month. This is in line with other studies. Intraoperative \ndetection of ureter injuries has been reported in only 5-13% of the cases 2, 7, 16. Among \nthe acute injuries of the urinary tract, ureter injuries are the most difficult to recognize \nas there often may be few or no symptoms 1. Indeed, in our cases only one patient \nhad a recognized protracted primary postoperative recovery and only one injury was \ndiscovered at the time of the primary surgery. Most of the surgeons do not apply standard \nadditional intra- or postoperative diagnostic screening methods, including intravenous \ndye injection, ultrasonography, or cystoscopy to assess ureteral outflow in the bladder, \nto exclude ureter injury. Whether these diagnostic methods would have identified all \nureter injuries in our cases is a matter of debate. Several studies proposed routine use of \nintraoperative cystoscopy to assess the ureter flow as a part of all LHs 17-19. Cystoscopy \nduring LH is well tolerated and can reassure surgeons of immediate urinary tract injuries, \nbut it is not useful in identifying patients who may later fistulize 18. Given the low incidence \nof ureter injuries, it is an additional time-consuming procedure that is not required in \nmost patients. Cystoscopy during LHs was postulated to be cost-effective if the rate of \n118\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nureter injury exceeded 2% 19. Thus, the agreed upon advise of the expert panel to apply \nadditional intraoperative ultrasound or cystoscopy only in patients with increased risk on \nureter injuries, i.e., patients with distorted anatomy or very large uteri, seems to be logical \nin terms of cost-effectiveness. Given the possible relation between ureter injuries and \nan incomplete learning curve of the primary surgeon, we should start a discussion on \nwhether intraoperative cystoscopy or Doppler ultrasound to assess ureteral flow should be \nperformed on a routine base during all LHs performed by surgeons during their learning \ncurve. It would be interesting to calculate the number needed to diagnose; however, this \nwas not possible in our study given the lack of baseline characteristics of patients who \nhad LHs in the past 20 years in the Netherlands without an ureter injury. Because of the \nretrospective design of this study and the presence of a recall bias, the total reported \nnumber of injuries should be considered incomplete. This also underlines the need for \nprospective registration of all LHs, its baseline characteristics, and complications.\nIn conclusion, insufficient experience of the surgeon with the applied technique and \ndistortion of the anatomy by pelvic disease (e.g., endometriosis) are predisposing factors \nfor ureter injuries. The earlier agreed upon recommendations by the Delphi study, such as \nthe relevance of surgical experience of the surgical team, the use of an uterine manipulator, \ncoagulation of the uterine pedicles from the ipsilateral side, and complete ureterolysis in \ncase of distorted anatomy, are confirmed in this study. In addition, intraoperative cystoscopy \nor sonography to assess ureteral flow should be considered in these cases. Based on the \nprevious Delphi study and on the current study, we propose recommendations in order to \nprevent ureter injuries during LHs and to promote its early detection (Table 5).\nTable 5. Recommendations by the authors for performing the laparoscopic hysterectomy with respect to \npreventing ureter injuries\nPreoperatively\n1 Completion of learning curve (i.e., at least 30) with tutor (surgeon with sufficient experience and \nqualifications)\nIntraoperatively\n2 Use appropriate instruments: e.g., uterus manipulator\n3 Coagulate uterine vessels close to the uterus from ipsilateral side with a perpendicular approach; \ni.e., minimizing risk on bleeding and enlarge distance between uterine artery and ureter\n4 Completea ureter visualization in case of distorted anatomy before coagulation can take place\nPostoperatively\n5 In case of distortion of anatomy and/or bleeding, performing cystoscopy during surgery or Doppler \nultrasound ureteral flow on first postoperative day\n6 Before completion of the learning curve, perform recommendation no. 5 in all cases, also in case of \nnormal anatomy\nGeneral recommendation\n7 Nationwide prospective registration of all operative procedures, including baseline characteristics \nand complications\na Complete is defined as visualization of the ureter in the course of the operation field (in the pelvis). This \nincludes opening of the peritoneum and, if required, ureterolysis\n119\n\nANALYSIS OF URETER INJURIES DURING LAPAROSCOPIC HYSTERECTOMY\n7\nACKNOWLEDGEMENTS\nWe are very grateful to the participating gynecologists for reporting their cases and \ncollaborating in the analysis.\nREFERENCE LIST\n1. Onwudiegwu U, Makinde OO, Badejo OA, Okonofua FE, Ogunniyi SO. Ureteric injuries \nassociated with gynecologic surgery. Int J Gynaecol Obstet 1991; 34(3):235-238.\n2. Harkki-Siren P , Sjoberg J, Tiitinen A. Urinary tract injuries after hysterectomy. Obstet Gynecol \n1998; 92(1):113-118.\n3. Makinen J, Johansson J, Tomas C et al. Morbidity of 10 110 hysterectomies by type of \napproach. Hum Reprod 2001; 16(7):1473-1478.\n4. Saidi MH, Sadler RK, Vancaillie TG, Akright BD, Farhart SA, White AJ. Diagnosis and \nmanagement of serious urinary complications after major operative laparoscopy. Obstet \nGynecol 1996; 87(2):272-276.\n5. Wattiez A, Soriano D, Cohen SB et al. 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