How does visceral obesity affect surgical performance in laparoscopic radical nephrectomy?

Japanese Journal of Clinical Oncology, 2015, 45(4) 373 377 doi: 10.1093/jjco/hyv001 Advance Access Publication Date: 30 January 2015 Original Article Original Article How does visceral obesity affect surgical performance in laparoscopic radical nephrectomy? Kazuyuki Yuge, Akira Miyajima*, Masahiro Jinzaki, Gou Kaneko, Masayuki Hagiwara, Masanori Hasegawa, Toshikazu Takeda, Eiji Kikuchi, Ken Nakagawa, and Mototsugu Oya Department of Urology and Diagnostic Radiology, Keio University School of Medicine, Tokyo, Japan *For reprints and all correspondence: Akira Miyajima, Department of Urology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. E-mail: akiram@a8.keio.jp Received 24 September 2014; Accepted 2 January 2015 Abstract Objective: In a previous study, we described the relationship between operating time and obesity, particularly visceral obesity, in laparoscopic surgery. Operating time in laparoscopic surgery is affected by the experience and technique of the surgeon. Here, we investigated whether a difference in the surgeon s experience affects the operating time for laparoscopic radical nephrectomy in patients with visceral obesity. Methods: From January 2006 to February 2012, 167 laparoscopic radical nephrectomies were performed at our institution. Visceral fat area was measured at the level of the umbilicus using computed tomography. A visceral fat area 100 cm 2 was used as the definition of visceral obesity. All laparoscopic radical nephrectomies were performed by six surgeons. Two of the six surgeons perform 50 cases or more laparoscopic surgeries every year and they were defined as the expert group. We analyzed the relationships between clinical findings, methods, surgeon experience, body mass index or visceral fat area and operating time. Results: The expert and non-expert surgeons performed 77 and 90 laparoscopic radical nephrectomies, respectively, and the median operating time was 167.0 ± 44.0 and 227.5 ± 60.6 min. Twenty-five patients underwent laparoendoscopic single-site nephrectomy by the expert surgeons. For all surgeons, visceral obesity was a significant factor for prolonged operating time. Multivariate analysis showed that visceral obesity and clinical T stage were independent risk factors for prolonged operating time for the non-expert surgeons [P = 0.004, hazard ratio (HR): 5.15, P = 0.037, HR:10.41]. However, for the expert surgeons, clinical T stage was the only independent risk factor for prolonged operating time (P = 0.039, HR: 4.33). Conclusion: Visceral obesity was a factor of prolonged operating time in laparoscopic radical nephrectomy. The non-expert surgeons were particularly affected by visceral obesity. Key words: visceral obesity, laparoscopic nephrectomy, expert, operating time The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com 373

374 Visceral obesity affects LRN s performance Introduction Obesity has become a major social and health issue not only in industrialized nations but also developing countries (1), and is a risk factor for various diseases, such as diabetes mellitus, hypertension, coronary heart disease, airway obstruction and malignant tumors (2). In the past, obesity was thought to be a relative contraindication to laparoscopy (3); laparoscopic nephrectomy becomes technically more difficult as body mass index (BMI) increases (4), however, because the prevalence of obesity is increasing, more overweight patients are now being considered for laparoscopic surgery. In general, obesity is thought to be a major factor influencing the degree of technical difficulty of a surgical procedure (5,6). Previous studies have reported that the complication rates for urological laparoscopic surgery in obese patients were higher than those in patients of normal weight (1,3), therefore, it was believed that obesity was a relative contraindication to laparoscopy. Several recent studies in the literature, however, have reported on the safety of laparoscopic radical nephrectomy (LRN) for obese patients by comparing complication rates with those for non-obese patients (7 11). In a previous study, we reported that LRN in patients with a high BMI could be performed more safely than open-radical nephrectomy (ORN) (4). We also reported using visceral fat area (VFA) as an index of visceral obesity, and that it was a better factor of prolonged operating time than BMI in LRN (12). Laparoscopic nephrectomy was first introduced in 1991 by Clayman et al. (13) for benign renal disease. Since then, LRN has become firmly established as the preferred management technique for T1 and selected T2 RCCs (14 16). The criteria for LRN have now been expanded to T3a with greater surgeon experience (17). LRN is now performed in many countries by urologists with a lot of experience as well as those with less experience. We believe that surgeons with little experience require further training since the surgical outcomes and risk of complications are worse. Inexperienced operators should select an operating method and strategy that will ensure a safe and successful operation. Therefore, we sought to identity factors that affect surgical outcome in terms of surgeon experience. The aim of the present study was to determine whether visceral obesity affects surgeons who are either experienced or inexperienced. We also attempted to determine whether adequate surgical experience can overcome the problems associated with visceral obesity. Patients and methods We performed a retrospective analysis of data obtained from patients who had undergone LRN from January 2006 to February 2012 at our institution. A total of 167 LRNs were performed for T1 and selected T2, T3a or T3b RCCs and benign disease (oncocytoma, angiomyolipoma or chronic nephritis). All laparoscopic nephrectomies were performed using the transperitoneal approach. Beginning in September 2009, some of the LRNs were performed by laparoscopic single-site surgery (LESS) at our institution. The decision concerning whether to perform conventional LRN or LESS was made by the attending physician. All LRNs were performed by six urologists. Two of the six urologists had continuously performed 50 or more laparoscopic surgeries (adrenalectomy, radical nephrectomy, partial nephrectomy or radical prostatectomy) every year. We defined these two urologists as expert surgeons, while the other four urologists were defined as non-expert surgeons. VFA was measured at the level of the umbilicus using pre-operative CT according to a procedure described and validated previously. The tomographic attenuation of the adipose tissue was defined to be Figure 1. Computed tomography showing the degree of fat distribution. The green area within the drawn circle is the visceral fat area. between 50 and 150 HU. The border of the intraabdominal cavity was outlined on the CT image, and VFA was then quantified using standard software (Fig. 1). One radiologist completed all the measurements and was blinded to the clinical details of the subjects. According to previous study, VFA 100 cm 3 is a diagnostic criteria for visceral obesity (18). Therefore, VFA was classified as visceral obesity (high VFA; VFA 100 cm 2 ) or non-visceral obesity (low VFA; VFA < 100 cm 2 ). BMI was calculated for all patients. Data were collected according to institutional review board protocol (Approval no. 2011-301). The relationships between each clinical variable, for example, age, gender, laterality, tumor size, clinical T stage, method of LRN, BMI or VFA and operating time were analyzed using a χ 2 test for categorical variables, respectively. Multivariate analyses using logistic regression were performed to identify the risk factors associated with a prolonged operating time in LRN. In these analyses, the mean of operating time for laparoscopic nephrectomy was used as a threshold value, regardless of whether the operating time was long or not. The mean (SD; range) operating time was 199.6 (61.4; 95 484) min. A P value of <0.05 was considered to indicate statistical significance. The analyses were performed using SPSS, version 17.0 (SPSS Inc., Chicago, IL, USA). Results A total of 167 patients underwent LRN. World Health Organization (WHO) classifies BMI into three categories (healthy weight: BMI < 25.0 kg/m 2, overweight: 25.0 kg/m 2 BMI < 30.0 kg/m 2 and obese: BMI 30.0 kg/m 2 ). The mean (SD) BMI of the patients was 23.8 kg/m 2 (3.7); 69.5% of the patients were classified as healthy weight, 25.1% as overweight and 5.4% as obese. The mean (SD) VFA at the umbilicus level determined by CT was 121.6 (68.4) cm 2. There were 99 patients (59.3%) with visceral obesity. Twelve patients with benign renal disease underwent LRNs, including 3 oncocytoma, 6 angiomyolipoma and 3 chronic pyelonephrosis. The mean age of all cohorts was 58.3 years (range, 32 87 years). Males accounted for 72.5% (121 patients) and females 27.5% (46 patients). Laterality was the right side in 72 cases and the left side in 95 cases. In the 155 cases with renal cell carcinoma, the stage was clinical T1a, T1b, T2a, T2b, T3a and T3b in 89, 39, 15, 2, 9 and 1 case, respectively. Twenty-five LESSs were performed by the expert surgeons.

Jpn J Clin Oncol, 2015, Vol. 45, No. 4 375 Table 1 presents the patient characteristics, operative data and demographics between the expert and non-expert surgeons. The two expert surgeons performed LRNs in 77 patients. The mean (SD; range) operating time was 167.0 (44.0; 95 259) min in the expert group and 227.5 (60.6; 134 484) min in the non-expert group. Operating time, age and method of operation were significantly different between the two groups (P < 0.001, 0.036 and <0.001, respectively). We analyzed the factors of a prolonged operating time in the expert and non-expert surgeon groups. Age ( 60 or <60 years), gender, laterality, tumor size ( 4.0 or <4.0 cm), clinical tumor stage ( ct2a or ct1b), method of operation (conventional laparoscopic surgery or LESS), BMI ( 25 kg/m 2 : high BMI group or <25 kg/m 2 :normal group) and VFA (visceral obesity or non-visceral obesity) were used to divide the patients into two categories. In the non-expert surgeon group, multivariate logistic regression analysis demonstrated that clinical tumor stage ( ct2a) and VFA (visceral obesity) were independent factors for a prolonged operating time (P =0.037, HR: 10.129, P = 0.004, HR: 5.12, respectively; Table 2). Meanwhile, in the expert surgeon group, only clinical tumor stage ( ct2a) was an independent factor (P = 0.039, HR: 4.33; Table 3). The mean volume of intraoperative bleeding was 39.0 (SD; 92.5; range; several ml to 500) ml. The incidences of intraoperative or postoperative complications were as follows; one case of colon injury, 18 Table 1: Clinical variable in the 167 study patients By expert surgeon By non-expert surgeon P value No of patients: 77 90 Patients with benign disease: 3 9 Mean (SD) age (years old): 60.5±12.5 56.4±12.3 0.036 Age: 0.037 <60 years 32 52 60 years 45 38 Gender: 0.784 Male 55 66 Female 22 24 Tumor laterality: 0.316 Right 30 42 Left 47 48 Tumor size: 0.800 <4.0 cm 44 48 4.0 cm 33 39 Clinical T stage: 0.220 ct1a 44 45 ct1b 20 19 ct2a 3 12 ct2b 1 1 ct3a 6 3 ct3b 0 1 Method of laparoscopic <0.001 radical nephrectomy: Traditional 52 90 LESS 25 0 Mean (SD) BMI (kg/m 2 ): 23.8±3.8 23.7±3.7 0.853 BMI: 0.862 <25 kg/m 2 54 62 25 kg/m 2 23 28 Mean (SD) VFA (cm 2 ): 124.8±67.4 118.9±69.6 0.584 VFA: 0.743 <100 cm 2 31 34 100 cm 2 46 56 Operating time (min): 167.0±44.0 227.5±60.6 <0.001 cases of urinary retention and 1 case of wound dehiscence. However, none of the patients required transfusion or open conversion. Discussion In the present study, a high tumor stage ( ct2a) and high VFA (visceral obesity) were risk factors for a prolonged operating time. In multivariate analysis, only a high tumor stage was an independent factor for the expert surgeons. However, a high tumor stage and a high VFA were independent factors for the non-expert surgeons. Of particular interest is the fact that the cases operated on by expert surgeons included 25 cases of LESS. This suggests that more experienced surgeons are not as easily affected by visceral obesity as inexperienced surgeons. LRN is increasingly being performed and has become the standard technique not only for low stage RCCs but also high stage RCCs. At our institution, LRN was performed in 10 cases with ct3 RCC. In the present study, high stage RCC was an independent risk factor for prolonged operating time for both the expert and non-expert surgeons. This suggests that LRN in cases with high stage RCC is always difficult, regardless of the level of experience of the surgeon. This analysis demonstrated that visceral obesity was an independent risk factor for prolonged operating time for non-expert surgeons. Meanwhile, among expert surgeons, visceral obesity tended to affect operating time, but it was not an independent risk factor. Previous reports examined whether a high BMI influences surgical outcomes. Anast et al. (7) compared 12 obese patients (BMI 30 kg/m 2 )and 32 non-obese patients (BMI < 30 kg/m 2 ) undergoing LRNs and reported that the obese group had significantly longer operating times than the non-obese group. Miyake et al. (19) concluded that LRN became more difficult with increasing BMI after taking into consideration the overall trends toward longer operating times. However, Table 2: Risk factors for prolonged operating time by non-expert surgeons using univariate and multivariate analyses. Logistic regression analysis of prolonged operating time Univariate Multivariate P value HR (95%CI) P value Age: 0.791 0.883 <60 years 60 years Gender: 0.076 0.326 Male Female Tumor laterality: 0.116 0.246 Right Left Tumor size: 0.127 0.709 <4.0 cm 4.0 cm Clinical T stage: 0.034 0.037 ct1b ct2a 10.417 (1.19-90.70) BMI: 0.158 0.422 <25 kg/m 2 25 kg/m 2 VFA: 0.007 0.004 <100 cm 2 100 cm 2 5.15 (1.68-15.78)

376 Visceral obesity affects LRN s performance Table 3: Risk factors for prolonged operating time by expert surgeons using univariate and multivariate analyses. Logistic regression analysis of prolonged operating time Univariate Multivariate P value HR (95%CI) P value Age: 0.602 0.717 <60 years 60 years Gender: 0.602 0.719 Male Female Tumor laterality: 0.832 0.513 Right Left Tumor size: 0.039 0.074 <4.0 cm 4.0 cm Clinical T stage: 0.029 0.039 ct1b ct2a 4.33 (1.08-17.39) Method of laparoscopic 0.146 0.117 radical nephrectomy: Traditional LESS BMI: 0.249 0.376 <25 kg/m 2 25 kg/m 2 VFA: 0.111 0.133 <100 cm 2 100 cm 2 Feder et al. (8) reported that there was no significant difference in operating time or estimated blood loss with increasing BMI in patients undergoing LRN. We previously evaluated the effect of BMI on radical nephrectomy and partial nephrectomy (4,20) and concluded that laparoscopic surgery for patients with a high BMI is safer than open surgery. The present study demonstrates that VFA significantly prolongs operating time. This tendency was particularly obvious in the performance of the non-expert surgeons. This suggests that experience may be able to overcome VFA in LRN. Therefore, when a non-expert surgeon performs radical nephrectomy in a patient with high VFA, he or she should carefully consider the method and strategy of the operation. It is preferable that a surgery be safe and as short as possible. However, the skill and experience of the surgeon are risk factors for a prolonged operating time, and for an inexperienced surgeon further improvement in skills is difficult without experience at laparoscopic surgery (21,22). For this reason, inexperienced surgeons, especially trainees, should carefully select a surgical method and strategy for laparoscopic surgery on a case-by-case basis. We believe it is helpful to ascertain which type of surgery can be performed safely by determining beforehand what kind of case may potentially make the surgery difficult to perform. This study has several limitations. First, it was performed in a retrospective manner, and unknown sources of bias may exist in the findings. Due to the limited sample sizes for both patients and surgeons, a detailed evaluation was not possible. Moreover, LESS has a very similar operative process to traditional LRN, with the only difference being the single port. However, the operative difficulty of LESS was greater than that of traditional LRN. Therefore, the analysis that excluded the LESS cases from the expert group was the best. However, because the patients with ct2 or more tumors underwent LESS in the expert group, the patients were included in our database. Second, there were only nine patients with a BMI >30.0 kg/m 2 in the present study. In studies from other countries, there were more patients with a high BMI (BMI 30 kg/m 2 ). BMI is the index usually used to evaluate obesity. Previous reports often used BMI as the index of obesity and various cut-off points for BMI were used. In the present study, we defined patients with a BMI >25.0 kg/m 2 as obese based on the recommendation for Asian people of the Western Pacific Regional Office of the WHO (23). However, BMI does not accurately reflect all types of obesity. We reported that VFA as an index of visceral obesity had a stronger correlation with a prolonged operating time than BMI in LRN (12). Therefore, whether or not the present result is applicable to patients from other countries is still not clear and needs to be validated. However, the aim of the present study was not to compare the surgical outcome between obese and non-obese patients, but rather to evaluate what factors are associated with surgical outcome in relation to surgeon experience. 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