Archivio Italiano di Urologia e Andrologia 2017; 89, 4266 ORIGINAL PAPER Evaluation of the complications in laparoscopic retroperitoneal radical nephrectomy; An experience of high volume centre Ali Serdar Gozen 1, Vitalie Gherman 1, 3, Yigit Akin 1, Mustafa Suat Bolat 1, Muhammad Elmussareh 2, Jens Rassweiler 1 1 Department of Urology, SLK-Kliniken, University of Heidelberg, Heilbronn, Germany; 2 Department of Urology, Mid Yorkshire Hospitals NHS Trust, Wakefield, UK; 3 Department of Urology, “Iuliu Hatieganu” University of Medicine and Pharmacy, Cluj-Napoca, Romania. Objectives: To provide a standardised report of complications after retroperitoneal laparoscopic radical nephrectomy (rLRN) in a high-volume centre using Clavien-Dindo classification. Materials and methods: We analysed records maintained in a prospective database of 330 consecutive patients that under- went rLRN between March 1995 and September 2016. All complications were graded according to the modified Clavien-Dindo classification. Three generations of surgeons were defined and the learning curve in rLRN was evaluated by comparing the first 100 cases (Group A) performed by first- generation surgeons with the last 100 cases (Group B) by third- generation surgeons. Results: The mean age of our cohort was 66 ± 11.9 years. The overall complication rate was 19.7%. The majority of com- plications (12.7%) were Clavien 1 (5.1%) and Clavien 2 (7.6%) and did not require any interventions; blood transfusion was the most frequently encountered intervention (4.8%). Half of which were because of major intraoperative bleeding. Mortality rate was 0.9%. We found a trend towards lower complication rate in group B (19%) compared to group A (23%); this was mainly because of the reduction in the incidence of Clavien 1 and 2 complications. The pathological stage varied significantly in the two groups while the rate of negative surgical margins was comparable. Conclusions: rLRN is a safe procedure with an acceptable rate of complications. The learning curve was shorter for the third- generation surgeons (group B); although these surgeons operat- ed on a significantly higher number of patients with more advanced diseases. The Clavien-Dindo classification is suitable for assessing rLRN complications. Adopting this standardised system can help in the evaluation and comparison of surgical quality of LRN series. KEY WORDS: Laparoscopy; Kidney cancer; Complications; Clavien-Dindo classification. Submitted 19 July 2017; Accepted 3 August 2017 Summary No conflict of interest declared. kidney (1). Radical nephrectomy (RN) remains the gold standard surgical treatment for patients with RCC when nephron-sparing procedures are not feasible (2). Over the past two decades, with advancements in laparoscop- ic surgery, laparoscopic RN (LRN) has become a widely available surgical option that has been shown to provide similar oncological outcomes to open surgical tech- niques with the well-known benefits of laparoscopic approach (3-5). At present, it is regarded as a standard treatment worldwide with up to 80% of urologists offer- ing LRN to patients with localised RC (6). LRN can be performed by two different approaches, namely the retroperitoneal route or the transperitoneal route. The retroperitoneal approach, which was developed to mimic open-flank nephrectomy, allows rapid and direct access to the renal pedicle without violating the peri- toneal cavity. Thus, retroperitoneal LRN (rLRN) can minimise the risk of some complications, such as viscer- al organ injuries. The European Guidelines on Reporting and Grading of Complications After Urologic Surgical Procedures were recently published (7). The key recom- mendations of these guidelines include the use of a stan- dardised system, such as the Clavien-Dindo grading sys- tem (8), and the provision of a table of all complications and corresponding scores or a list of the complications by scores. Complication rates are still one of the most frequently used surrogate indicators for the quality of surgery. However, to the best of our knowledge, no data have been published on rLRN complications using stan- dardised classifications. In this study, we report on our large, single-institution rLRN series, representing over 15 years of experience. The purpose of the study is to determine the complication rates after rLRN using a standardised method, namely the Clavien-Dindo classifi- cation, in a large cohort at a pioneering institution. MATERIALS AND METHODS Between March 1995 and September 2016, 380 consec- utive LRN surgeries were performed for patients with renal tumours (stage T1-T4) at our institution. All patients were counselled appropriately about the treat- DOI: 10.4081/aiua.2017.4.266 INTRODUCTION Renal cell carcinoma (RCC) is the most common malig- nant tumour of the kidney parenchyma, representing approximately 2% of all new cases of cancer and accounting for over 80% of all neoplasms that affect the Gozen_Stesura Seveso 03/01/18 11:01 Pagina 266 267Archivio Italiano di Urologia e Andrologia 2017; 89, 4 Complications in laparoscopic nephrectomy ment and the aim of this study with written informed con- sent obtained prior to the surgery. In our centre, the pre- ferred laparoscopic approach is the retroperitoneal route which was first described by Gaur (9) and later modified and developed by Rassweiler et al. (10, 11). All data were recorded prospectively using a Microsoft Office Excel spreadsheet. We excluded cases that were performed via transperitoneal laparoscopic approach or open surgery, those with less than 12 months of follow- up or missing follow-up data and patients with addition- al cancer or bilateral renal tumours. Thus, 330 patients with complete follow up were enrolled in the study. The review board of our certified cancer centre approved our prospective collection of patients’ data. In the first 50 cases, the specimen was entrapped in an organ retrieval bag and extracted via a flank incision without prior morcellation. Afterwards, we preferred to extract the specimen through a Gibson incision. All patients stayed in the intensive care unit (ICU) for the first 24 hours after the operation and received antibiotics for a minimum of 3 days in the postoperative period. Three generations of surgeons were defined as follows: first-generation surgeons had previous experience in open surgery but no laparoscopic training; second-gener- ation surgeons had experience in open surgery, and they were trained by first-generation surgeons; and third-gen- eration surgeons had no or limited experience in open surgery, and they were trained by first-or second-genera- tion surgeons (12). The learning curves of the first- and third-generation surgeons were compared and analysed based on the results of the first 100 and last 100 cases. Data collection Demographic data, including age (years), gender, co- morbidities, body mass index (BMI; kg/m2), operation history, tumour size (mm), tumour side and preopera- tive clinical stage, were recorded. Operative and postop- erative data, including operation time; estimated blood loss; conversion to open surgery; length of hospital stay and duration of surgical drains; were also noted. All pathological specimens were reviewed by a single, expe- rienced pathologist; the pathology results, including tumour staging, were evaluated according to the revised 2009 TNM classification (13). Complications were noted in detail, including treatment and outcomes, as part of our internal quality management system. Complication assessments and follow-up schedule All the charts, including the medical records, of patients with identified postoperative complications were reviewed and grouped according to the modified Clavien-Dindo classification (Table 1). Medical and surgical complica- tions during the first 6 weeks were evaluated at the end of this period using our institution’s medical records and reports from the rehabilitation centre and other physi- cians. Patients were followed up every 3 months for the first 2 years after surgery then 6 monthly thereafter. Statistical analyses All data were recorded in Microsoft Excel files. For sta- tistical analysis, we used a commercially available soft- ware package (SPSS v16.0; SPSS, Chicago, IL, USA) Table 1. Complication assessment according to modified Clavien-Dindo classifications. Grade Definition Clavien 1 Any deviation from the normal postoperative course without the need for pharmacological treatment or surgical, endoscopic and radiological interventions. Acceptable therapeutic regimens are: drugs as anti-emetics, antipyretics, analgesics, diuretics and electrolytes and physiotherapy. This grade also includes wound infections opened at the bedside. Clavien 2 Complications requiring pharmacological treatment with drugs other than such allowed for grade I complications. Blood transfusions and total parenteral nutrition are also included. Clavien 3a Complications needing surgical, endoscopic, or radiologic intervention under local anaesthesia. Clavien 3b Complications needing surgical, endoscopic, or radiologic intervention under general anaesthesia (including dialysis). Clavien 4a Life-threatening complications requiring ICU management: single organ dysfunction. Clavien 4b Life-threatening complications requiring ICU1 management: multiorgan dysfunction. Clavien 5 Death of the patient. Suffix ’d’ If the patient suffers from a complication at the time of discharge, the suffix “d” (for ‘disability’) is added to the respective grade of complication. This label indicates the need for a follow-up to fully evaluate the complication. ICU1 = Intensive care unit. including the Pearson X2 test. A p-value < 0.05 was con- sidered statistically significant. RESULTS Patient clinico-pathological characteristics and distribution of complications This study included 330 patients who underwent rLRN performed by one of six surgeons at a single centre. The median follow-up time was 33 ± 9.8 months. Demographic, intraoperative and pathological data are presented in Table 2. Seventy-three postoperative complications were identi- fied in 63 patients (19.1%). In 52 patients (82.5%), only one complication was recorded, while 11 patients (17.5 %) had two or more complications. As recommended by Dindo et al. (8), when one complication was clearly relat- ed to another, only the more severe one was labelled and reported. Hence, we reported a complication rate of 19.7% (65 complications), as eight patients had received concomi- tant blood transfusion with more severe complications (four conversions and four open revisions). Minor complications that needed no or non-intervention- al treatments represented 12.7% of all those reported (Clavien 1: 5.1%; Clavien 2: 7.6%; Table 1). Complications requiring reintervention with or without anaesthesia occurred in 6% of cases (Clavien 3a: 1.5%; Clavien 3b: 2.1%; Clavien 4a: 2.1%; Clavien 4b: 0.3%). The mortality rate was 0.9% (Clavien 5). The conversion rate was 2.1%, with half the cases requir- Gozen_Stesura Seveso 03/01/18 11:01 Pagina 267 Archivio Italiano di Urologia e Andrologia 2017; 89, 4 A. Serdar Gozen, V. Gherman, Y. Akin, M. Suat Bolat, M. Elmussareh, J. Rassweiler 268 ing open conversion because of uncontrollable intraoper- ative bleeding. The most frequent complication was anaemia requiring transfusions, which occurred in 4.8% of cases. Detailed information on each category of compli- cations and their management is presented in Table 3. Analysis of the learning curve To analyse the learning curves of the first- and third-gen- eration surgeons, we compared the first 100 cases (group A) with the last 100 cases (group B). There was no signifi- cant difference in demographic data in these groups (Table 4); the intraoperative records were also similar. The operative time was comparable between the two groups (135 min vs. 128 min in group A and group B, respectively), with no significant difference in average tumour size (46 mm vs. 62 mm) or estimated blood loss (140 ml vs. 100 ml). There was, however, a significant difference in pathologi- cal tumour stage between the two groups. In group A, 73% (68 patients) of patients that had malignant patholo- gy were found to have pT1-tumours compared to only 30% of cases in group B. Whereas, third-generation sur- geons treated significantly more patients with pT3 disease (45.6% vs. 12.9%; p < 0.001). Despite the increased com- plexity of cases performed by the last generation of sur- geons, the rates of negative surgical margins were similar in both groups (98.9% vs. 94.6%), and the total compli- cation rates were comparable (23% vs. 19%), (p = 0.04%). The conversion rates were similar in both groups, while blood transfusion rates were higher in the first 100 cases. This trend in reduction of overall complication rates was mainly because of the lower incidence of Clavien 1 and Clavien 2 complications (blood transfu- sions, infections, etc.) (Figure 1). The complication rates were higher for the first 40 cases in the first group and the first 25 cases in the second group. Complication rates and institutional learning curves are also influ- enced by technical and technological developments over time. DISCUSSION In the present study, we summarised rLRN complications according to the Clavien-Dindo classification. To the best of our knowledge, this is the first detailed report on this issue. It is well-accepted that successful operative and patients’outcomes can be supported through standard- ised postoperative complication classifications. Comparison with other series In 2004, the Clavien-Dindo classification system for reporting postoperative complications was introduced and successfully validated in general surgery (8). It has been successfully employed in case series for reporting complications in urological procedures such as transurethral prostate resection; percutaneous nephrolithotomy; laparoscopic live-donor nephrecto- my; and laparoscopic, robotic-assisted and retropubic radical prostatectomy (12, 14-20). However, after more than a decade, it is still not frequently used in all fields of minimally invasive urological surgeries. Using the modified Clavien- Dindo classification, we observed a compli- cation rate of 19.7% in a prospective series of 330 consecutive rLRN. Abbou et al. (5) reported similar findings: their rLRN over- all complication rate was 8%. However, they may have observed lower complica- tion rates because they used the old version of the Clavien classification system. Similarly, Gill et al. (21) observed a compli- cation rate of 13% in a series of 34 rLRN sur- geries for suspected kidney cancer. The complications in this study were only Table 2. Demographic, operative and postoperative data of patients. Age (year) Mean (± SD): 66 ± 11.9 Gender Male: 207 (62.7%), Female: 123 (37.2%) BMI1, kg/m² (%) ≤ 25 (normal weight): 141 (42.7%) 26-30 (obesity I°): 133 (40.3%) 31-40 (obesity II°): 47 (14.2%) > 41 (obesity III°): 9 (2.7%) Mean BMI (± SD): 27.1 ± 5.1 Tumour side: Left: 177 (53.6%), Right: 153 (46.3%) Tumour size (mm): Mean (± SD): 58 ± 15.3 Range: 30-120 Operation time (min): Mean (± SD): 143 ± 46.3 Mean Estimated Blood Loss (ml): 155 Blood transfusion rate: 32 (9.6%) Concomitant adrenalectomy 154 (46.6%) Tumour histology Clear cell RCC2 - 254 (76.9%) Papillary - 26 (7.9%) Chromophobe - 12 (3.6%) TCC3 - 5 (1.5%) Other malignancies - 8 (2.4%) Benign - 25 (7.5%; Oncocytoma - 14 [4.2%]) Pathological T stage (pT), no. (%) pT1 - 147 (48.2%) pT2 - 62 (20.3%) pT3 - 89 (29.2%) pT4 - 7 (2.3%) Fuhrman grade, no. (%) Fuhrman I - 54 (18.5%) Fuhrman II - 155 (53.1%) Fuhrman III - 73 (25%) Fuhrman IV - 10 (3.4%) Surgical margins, no. (%) NSM4 (R0) - 298 (97.7%) PSM5 (R1) - 7 (2.3%) BMI1: Body mass index; RCC2: Renal cell carcinoma; TCC3: Transitional cell carcinoma; NSM4: Negative surgical margin; PSM5: Positive surgical margin. Figure 1. Complication rates by grade in first and last 100 cases. Gozen_Stesura Seveso 03/01/18 11:01 Pagina 268 269Archivio Italiano di Urologia e Andrologia 2017; 89, 4 Complications in laparoscopic nephrectomy summarised as minor and major com- plications, without using a standard- ised classification system to define the complications; nevertheless, the study underlines rLRN’s feasibility, repro- ducibility and relatively low complica- tion rate compared to open retroperi- toneal approach. Finally, Clavien and Dindo (8) revised and externally validated the pre-exist- ing classification system for postopera- tive complications in 2004. The new system was considered to be simple, logical, reproducible, useful and com- prehensive. Permpongkosolet al. (22) used Clavien- Dindo classification to assess the com- plications associated with urological laparoscopic surgery. In this study, the authors observed a total complication rate of 22.1% after more than 2700 laparoscopic procedures. In the LRN group, complications occurred in 20% of the patients. Conversion to open surgery occurred in 2.9% (16 patients) of cases, while the mortality rate was 0.2%. We reported seven open con- versions (2.1%) that we graded as Clavien 3b. A collaborative review by Breda et al. (23) concluded that although the retroperitoneal approach has the disadvantage of a smaller working space with no anatomical landmarks, it offers the clear advantage of rapid and direct access to the renal hilum. In addition, as in our experi- ence, the incidence of adjacent organ injuries is extremely low. Most major intra operative complications encoun- tered in the retroperitoneal approach were related to vascular injuries. In previous studies, the complication rates ranged from 8 to 22% (5, 21-23). However, the common limitation of these studies is difficulty in comparing similar surgical techniques in terms of postoperative complications due to a lack of a consensus on reporting post- operative complications in the litera- ture. Because our study used a stan- dardised system, it can address this limitation. Another point to consider is that all these complication rates may show a learning curve (24). Indeed, rLRN has a relatively steep learning curve; we found that a surgeon could reach a plateau after 40 cases in the first generation, where as a third-gen- eration surgeon could reach a plateau after 25 cases. This shortening of the learning curve may have resulted from our standardized laparoscopic training Table 3. Detailed analysis of Clavien-Dindo complications. Complication Clavien grade 1 Surgical site hematoma Recurrent pain at surgical site Ileus Minor bladder tamponade Allergic exanthema Diarrhoea caused by antibiotics Pneumopericardium Urinary retention after catheter removal Subcutaneous emphysema Total n/N, (%) Clavien grade 2 Anaemia without additional complications Urinary tract infection Other site infection Persistent postoperative fever Total n/N, (%) Clavien grade 3a Infection of the surgical site/ delayed healing Recurrent nausea and vomiting, reflux oesophagitis grade 1 Acute gastritis, duodenal ulcer, due to an increased need for analgesics over time Total n/N, (%) Clavien grade 3b Major intraoperative bleeding (vascular injury, vena cava rupture) Intraoperative visceral injury Lymph nodes; Vena Cava adhesion Total n/N, (%) Clavien grade 4a Major postoperative bleeding (1 patient with intracerebral bleeding and left hemip hemiparesis) Cardiac decompensation, potentially lethal arrhythmias Allergic shock caused by changes in antihypertensive medication (Enalapril) Massive bleeding from oesophageal ulcers Total n/N, (%) Clavien grade 4b Asystole, acute renal failure, thrombocytopenia respiratory insufficiency Total n/N, (%) Clavien grade 5 Cardiogenic shock, perioperative NSTEMI3, acute renal failure Acute-on-chronic renal failure, SIRS4, left kidney infarct Fulminant pulmonary embolism 2nd day after the procedure Total n/N, (%) PPi1: Proton pump inhibitors, ICU2: Intensive care Unit, NSTEMI3: Non-ST segment elevation myocardial infarction, SIRS4: Systemic Inflammatory Response Syndrome. Management of complications No special therapy (topic ointment) Oral analgesics Laxatives, parenteral alimentation Bladder irrigation through catheter Antibiotic discontinuation Antibiotic discontinuation, fluid replacement, Imodium No special therapy Re-catheterization without cystoscopy No special therapy Transfusion Parenteral antibiotics Parenteral antibiotics Parenteral antibiotics Secondary suture Gastroscopy and PPi1 therapy (Esomeprazol 20 mg-7 days) Gastroduodenoscopy. PPi therapy (Pantoprazole 20 mg-5 days) Conversion Conversion Conversion Open revision, transfusions, treatment in ICU2 Implantation of a permanent cardiac pacemaker, treatment in the ICU Medical treatment in the ICU Endoscopic clipping of the bleeding sites, transfusion, treatment in ICU Successful cardio-pulmonary resuscitation, hemodyalisis, tracheostomy, artificial respiration, treatment in ICU Failed bradycardia resuscitation, circulatory insufficiency Failed cardio respiratory resuscitation Failed cardio respiratory resuscitation n, (%) 6 (1.8) 2 (0.6) 2 (0.6) 2 (0.6) 1 (0.3) 1 (0.3) 1 (0.3) 1 (0.3) 1 (0.3) 17/330 (5.1) 16 (4.8) 3 (0.9) 4 (1.2) 2 (0.6) 25/330 (7.5) 3 (0.9) 1 (0.3) 1 (0.3) 5/330 (1.5) 4 (1.2) 1 (0.3) 2 (0.6) 7/330 (2.1) 3 (0.9) 2 (0.6) 1 (0.3) 1 (0.3) 7/330 (2.1) 1 (0.3) 1/330 (0.3) 1 (0.3) 1 (0.3) 1 (0.3) 3/330 (0.9) Gozen_Stesura Seveso 03/01/18 11:01 Pagina 269 Archivio Italiano di Urologia e Andrologia 2017; 89, 4 A. Serdar Gozen, V. Gherman, Y. Akin, M. Suat Bolat, M. Elmussareh, J. Rassweiler 270 patient risk profile [comorbidities status, American Society of Anesthesiologists (ASA) score, tumour charac- teristics] and postoperative complications. This may be the subject of a future study. A further limitation of this study is that we only reported the standardised compli- cations of rLRN. The institutional learning curve may have a limited informative value because our data represent results from several surgeons working in a pioneering academ- ic training centre with residents and fellows attending certain procedural steps. CONCLUSIONS rLRN is a safe, reproducible technique associated with a relatively low incidence of complications. The learning curve was shorter for the third-generation surgeons; although these surgeons operated on significantly more patients with advanced diseases. 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Demographic, operative and postoperative data of first 100 cases and last 100 cases. Parameters Group A Group B p value (First 100) (Last 100) Age (years) 65 ± 12.6 67 ± 11.1 0.2 Gender 0.4 Male 59 66 Female 41 34 BMI (kg/m2) 0.5 ≤ 25 (normal weight) 46 41 26-30 (obesity I°) 42 44 31-40 (obesity II°) 9 10 > 41 (obesity III°) 3 5 Tumour size (mm) 46 ± 2.3 62 ± 3.2 0.3 Tumour side 0.4 Left 56 61 Right 44 39 Operation time (min) 135 ± 41.5 128 ± 43.4 0.2 EBL (ml) 140 ± 38.4 100 ± 43.7 0.5 Blood transfusion rate (n) 9 6 0.2 Tumour histology Clear cell RCC 84 71 0.5 Chromophobe 5 3 Papillary 2 9 TCC 2 6 Benign 7 7 Liposarcoma - 1 Metastasis - 2 Nephroblastoma - 1 Pathological T stage no. (%) 0.001* pT1 68 (73.1%) 27 (30%) pT2 13 (14%) 16 (17.8) pT3 12 (12.9%) 41 (45.6%) pT4 0 6 (6.5%) Fuhrman grade, no. (%) 0.07 Grade I 32 (35.2%) 10 (12%) Grade II 49 (53.8%) 44 (53%) Grade III 8 (8.8%) 21 (25.3%) Grade IV 2 (2.2%) 8 (9.6%) Surgical margins, no. (%) 5 (5.4%) NSM (R0) 92 (98.9%) 88 (94.6%) PSM (R1) 1 (1.1%) BMI: Body mass index, EBL: Estimated blood loss, RCC: Renal cell carcinoma, TCC: Transitional cell carcinoma, NSM: Negative surgical margin, PSM: Positive surgical margin. *Statistical Significant p value. programme supported by continuous technological development and improvement (25). We believe that our study can help beginners in laparoscopy, and the most experienced hands should also know about the standard- ised complication rates. Limitations of the study Our prospective database was created over a long peri- od of over 20 years. During this period, the Clavien clas- sification only changed twice. As such, the probability of bias in recording the complications is inherent. Minor complications (Clavien 1 and 2) could have been easily overlooked at the beginning of laparoscopic sur- gery when the method was emerging as a safe and viable alternative to open surgery. 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Complications of 2,775 urological laparoscopic procedures: 1993 to 2005. J Urol. 2007; 177:580. 23. Breda A, Finelli A, Janetschek G, et al. Complications of laparo- scopic surgery for renal masses: prevention, management, and com- parison with the open experience. Eur Urol. 2009; 55:836. 24. Rassweiler J, Fornara P, Weber M, et al. Laparoscopic nephrec- tomy: the experience of the laparoscopy working group of the German Urologic Association. J Urol. 1998; 160:18. 25. Furriel FTG, Laguna MP, Figueiredo AJC, et al. Training of European urology residents in laparoscopy: results of a pan- European survey. BJU Int. 2013; 112:1223. Correspondence Ali Serdar Gozen, MD, FEBU (Corresponding Author) Assoc. Prof. of Urology ali.goezen@slk.kliniken.de Vitalie Gherman, MD vitaliegherman@gmail.com Yigit Akin, MD yigitakin@hotmail.com Mustafa Suat Bolat, MD msbolat@gmail.com Jens Rassweiler, MD jens.rassweiler@slk-kliniken.de Department of Urology, SLK Kliniken Heilbronn, Am Gesundbrunnen 20-25, 74078 Heilbronn, Germany Muhammad Elmussareh, MD elmussareh@googlemail.com Department of Urology, Mid Yorkshire Hospitals NHS Trust, Wakefield, UK Gozen_Stesura Seveso 03/01/18 11:01 Pagina 271