Visceral obesity is a strong predictor of perioperative outcome in patients undergoing laparoscopic radical nephrectomy

Authors


Akira Miyajima, Department of Urology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. e-mail: akiram@a8.keio.jp

Abstract

Study Type – Therapy (case series)

Level of Evidence 4

What's known on the subject? and What does the study add?

Obesity is a common and growing problem in industrialized countries, and metabolic syndrome has been the focus of much attention recently, particularly with respect to obesity. Obesity is thought to be a major factor influencing surgical complexity during abdominal surgery, including laparoscopic surgery.

In this study, we focused on visceral obesity which has been recognized as the most important pathogenic factor in metabolic syndrome. We found that a high visceral fat area was a significant risk factor for a prolonged operating time. We believe that visceral obesity may greatly affect surgical complexity and may be a suitable index for predicting the degree of operating difficulty associated with laparoscopic nephrectomy.

OBJECTIVE

  • • To examine the impact of visceral fat on surgical complexity in patients undergoing laparoscopic nephrectomy.

PATIENTS AND METHODS

  • • We reviewed the medical records of 121 patients who underwent laparoscopic nephrectomy from 2006 to 2010 at our institution.
  • • The total fat area, visceral fat area (VFA) and subcutaneous fat area were measured at the level of the umbilicus using computed tomography (CT).
  • • To identify the type of obesity, we divided VFA into ≥100 cm2 and <100 cm2. A VFA ≥100 cm2 was used as the definition of visceral obesity.
  • • We evaluated the impact of the VFA on technical difficulties encountered during laparoscopic nephrectomy by measuring operating time.

RESULTS

  • • A significant correlation was observed between body mass index (BMI) and operating time (P < 0.001, r= 0.316) in the patients undergoing laparoscopic nephrectomy.
  • • VFA was also significantly correlated with operating time (P < 0.001, r= 0.348), and the correlation coefficient of VFA was higher than that of BMI.
  • • Multivariate analysis showed that a high VFA was an independent risk factor for prolonged operating time (P= 0.009, odds ratio; 3.70), whereas BMI was not found to be a risk factor.

CONCLUSIONS

  • • The present data indicate that measurement of VFA by CT is of benefit for predicting the technical difficulty associated with laparoscopic radical nephrectomy.
  • • Visceral obesity, which is one factor involved in metabolic syndrome, has a greater impact than BMI on the complexity of laparoscopic radical nephrectomy.
Abbreviations
TFA

total fat area

VFA

visceral fat area

SFA

subcutaneous fat area

BMI

body mass index

OR

odds ratio

PAI-1

plasminogen activator inhibitor type 1.

INTRODUCTION

Obesity is a common and growing problem in industrialized countries and even in some newly industrializing countries [1]. In the past, obesity was thought to be a relative contraindication to laparoscopy [2,3]; laparoscopic nephrectomy becomes technically more difficult as BMI increases [4], however, because the prevalence of obesity is increasing, more overweight patients are now being considered for laparoscopic surgery.

Laparoscopic nephrectomy was first introduced in 1991 by Clayman et al. for benign renal disease [5]. Since then, laparoscopic radical nephrectomy has become firmly established as the preferred management technique for T1 and selected T2 RCCs [6–8], and the criteria for laparoscopic radical nephrectomy have now been expanded to T3a with greater surgeon experience [9]. Laparoscopic radical nephrectomy is associated with lower analgesia requirements, a shorter hospital stay, and a quicker return to work than open procedures [10].

In general, obesity is thought to be a major factor influencing the degree of technical difficulty of a surgical procedure. 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 for obese patients by comparing complication rates with those for non-obese patients [11–15]. Previously, we also reported that for patients with a high BMI, the laparoscopic method was safe and of greater benefit than open nephrectomy [4]. Nevertheless, we recognized that although there was less of an impact in comparison with the open methods, laparoscopic nephrectomy, similarly to open nephrectomy, became technically more difficult as BMI increased [4].

Body mass index has often been used as a surrogate for obesity to predict the potential technical difficulties that might be encountered in laparoscopic nephrectomy, but obesity can now be classified according to visceral and subcutaneous obesity type, and visceral obesity has been recognized as the most important pathogenic factor of metabolic syndrome, the focus of much recent attention [16,17].

In the present study, we focused on visceral obesity and examined the impact of visceral obesity on technical difficulties in laparoscopic nephrectomy.

MATERIALS AND METHODS

We performed a retrospective analysis of data obtained from patients who had undergone laparoscopic nephrectomy at our institution. From January 2006 to October 2010, 121 laparoscopic radical nephrectomies were performed for T1 and selected T2 or T3a RCCs. Laparoscopic radical nephrectomy was not considered in patients with a tumour size >10 cm which was classified as T2b. All laparoscopic nephrectomies were performed using the transperitoneal approach.

Total fat area (TFA), visceral fat area (VFA) and subcutaneous fat area (SFA) were measured at the level of the umbilicus using CT according to a procedure described and validated previously [18–20]. The tomographic attenuation of the adipose tissue was defined to be between −50 and −150 HU. The border of the intra-abdominal cavity was outlined on the CT image, and TFA and VFA were then quantified using standard software (Fig. 1A,B). The SFA was calculated by subtracting VFA from TFA. One radiologist completed all the measurements and was blinded to the clinical details of the subjects. BMI was calculated for all patients. Data were collected according to institutional review board protocol (Approval no. 2011-301).

Figure 1.

CT showing the degree of fat distribution. A, Green area is the TFA. B, Green area is the VFA.

The relationships between each clinical variable, e.g. age, gender, laterality, location, tumour size, stage, BMI or VFA and operating time were analysed using a chi-squared test and t-test for categorical and continuous variables, respectively. One-way anova was used to compare the operating data if there were more than three groups. The correlation between continuous variables was investigated using Pearson's correlation coefficient. Multivariate analyses using logistic regression were performed to identify the risk factors associated with a prolonged operating time in laparoscopic nephrectomy.

In these analyses, the mean of each 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 192.3 (55.2; 95–367) 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 121 patients who had undergone laparoscopic radical nephrectomy were identified. According to the WHO classification, 71.8% of the patients were classified as having a healthy weight (BMI <25.0 kg/m2), 23.1% as overweight (BMI 25.0–29.9 kg/m2), and 4.1% as obese (BMI ≥30.0 kg/m2).

The mean (sd) TFA, VFA and SFA at the umbilicus level determined by CT were 267.7 (109.5) cm2, 122.6 (61.8) cm2 and 145.0 (67.8) cm2, respectively. VFA was then divided into ≥ or <100 cm2 in order to classify it as visceral obesity or non-visceral obesity.

Patient characteristics and demographics are shown in Table 1. There was significantly more visceral fat in males than females. There were no significant differences between the two groups in the other background factors but, in the intraoperative outcomes, the mean (sd) operating times in the visceral obesity group and the non-visceral obesity were 205.7 (57.5) min and 168.3 (42.6) min, respectively, and the difference was significant (P < 0.001). None of the patients in either group who had undergone laparoscopic radical nephrectomy required transfusion or open conversion.

Table 1. Patient characteristics and demographics
CharacteristicNo. of patientsVFA P
VFA <100 cm2VFA ≥100 cm2
Mean (sd) age 56.1(12.0)59.3 (12.2)0.172
Gender   <0.001
 Male902466
 Female312011
Laterality   0.168
 Left652045
 Right562432
Location   0.928
 Upper pole321121
 Middle pole552134
 Lower pole341222
Mean (sd) tumour size, cm 3.62 (1.67)3.90 (1.67)0.371
Clinical T category   0.885
 T1a722745
 T1b401327
 T2a422
 T3a523
Operating time 168.3 (42.6)206.0 (57.2)<0.001

Significant correlations were observed for BMI and operating time (P < 0.001, r= 0.316; Fig. 2). VFA also had a significant correlation with operating time (P < 0.001, r= 0.348; Fig. 3), and the correlation coefficient of VFA was higher than that of BMI.

Figure 2.

Scatter plot showing the relationship between BMI and operating time in laparoscopic radical nephrectomy.

Figure 3.

Scatter plot showing the relationship between VFA and operating time in laparoscopic radical nephrectomy.

Next, we divided the patients into a visceral obesity group in which the VFA was ≥100 cm2 and normal group in which the VFA was <100 cm2, and a high BMI group (BMI ≥25 kg/m2) and a normal group (BMI <25 kg/m2). Other factors, i.e. age (≥70 or <70 years), gender, tumour laterality, tumour location (upper, middle or lower pole), tumour size (≥4 cm or <4 cm), and clinical tumour stage (T1a, T1b, T2a, or T3a) were also used to divide the patients into two from four categories. Univariate analysis showed that sex, BMI and visceral obesity resulted in a prolonged operating time (Table 2). Multivariate analysis showed that high VFA was an independent risk factor for prolonged operating time (P= 0.009, odds ratio [OR]: 3.70). By contrast, BMI was not a risk factor (Table 2).

Table 2. Univariate and multivariate analyses of risk factors for prolonged operating time
CharacteristicNo. of patientsLogistic regression analysis
UnivariateMultivariate
P Hazard ratio (95% CI) P
Age 0.164  
 <70 years100
 ≥70 years21
Gender 0.006 0.101
 Male90
 Female31
Laterality 0.385  
 Left65
 Right56
Location 0.374  
 upper pole32
 middle pole55
 lower pole34
Tumour size 0.385  
 <4.0 cm65
 ≥4.0 cm56
Clinical T category 0.763  
 T1a72
 T1b40
 T2a4
 T3a5
BMI 0.044 0.956
 <25 kg/m287
 ≥25 kg/m234
VFA <0.001 0.009
 <100 cm244 
 ≥100 cm2773.70 (1.38–9.90)

DISCUSSION

Obesity is a common and growing problem in industrialized countries [1], and it is thought to be one of the risk factors for RCC [21–24]; patients with RCC often have a high BMI. Obese patients often have many medical conditions, such as cardiovascular disease, diabetes mellitus, and high blood pressure [25,26], factors which may affect surgical outcomes [27,28]. Many studies in the literature have used BMI as an indicator of the degree to which a patient is overweight, and BMI is often used as an indicator of physical frame; however, BMI does not always accurately reflect the various types of obesity because the distribution of adipose tissue differs greatly among individuals.

Many researchers have shown that excess visceral fat is more closely related than BMI to the risk of health problems such as type 2 diabetes and cardiovascular disease [29–34]. It has been suggested that a VFA ≥100 cm2 is the most sensitive and specific combination for detecting subjects with multiple risk factors, and is one of the diagnostic criteria for visceral obesity [35–37].

In the present study, linear regression analysis showed that BMI was significantly correlated with operating time (P < 0.001, r= 0.316) in patients undergoing laparoscopic nephrectomy. Significant correlations were also observed between VFA and operating time (P < 0.001, r= 0.348), and the correlation coefficient of VFA was higher than that of BMI. Multivariate analysis showed that a high VFA (≥100 cm2) was a significant risk factor for a prolonged operating time (P= 0.009, OR 3.70). By contrast, a high BMI (≥25 kg/m2) was not a significant risk factor. We believe this result indicates that, although obesity could cause the prolongation of operating time, visceral obesity, which is one of the factors used to diagnose metabolic syndrome, may have a stronger influence and may be a better index than BMI for predicting operating time.

Surgeons recognize that the level of visceral fat can have a significant influence on the difficulty of abdominal surgery, including laparoscopic nephrectomy. Visceral fat worsens the perioperative visual field and narrows the operating space, compared with subcutaneous fat. In addition, it has been reported that metabolic syndrome, which is defined as the presence of visceral obesity, is closely associated with slight chronic inflammation. Hypertrophied adipocytes in visceral fat secrete various cytokines and macrophages infiltrate the adipose tissue as a result of the increased production of cytokines. The infiltration of macrophages leads to slight chronic inflammation in adipose tissue and activates a network of inflammatory signalling pathways [38–41]. This inflammatory condition plays a critical role in metabolic syndrome, which is closely associated with blood lipid disorders, insulin resistance, and increased risk of developing type 2 diabetes and cardiovascular disease [38,42,43]. Meanwhile, several components of the inflammatory system, including the overexpression of cytokines and chemokines and the reduction of fibrinolytic activity, such as plasminogen activator inhibitor type 1 (PAI-1), have been shown to participate in adhesion formation [44]. PAI-1, a causative factor in the development of fibrosis leading to adhesion [44,45], is also increased in visceral fat by inflammatory mediators secreted from adipocytes, macrophages, and other immune cells in metabolic syndrome [40,41]. It is thought that slight chronic inflammation in adipose tissue affects perirenal fat, a component of visceral fat, which may cause its own fibrous adhesion and make perioperation manoeuvres more difficult in patients with metabolic syndrome. We believe the aforementioned effects of visceral fat extend the operating time and complicate the surgical procedure.

The most common technique used in the diagnois of RCC is CT [46] and VFA can be measured using CT. We believe that measurement of VFA is suitable for predicting difficulty associated with laparoscopic nephrectomy, because it does not require an additional examination. The present study is the first article to describe the correlations between visceral obesity, metabolic syndrome and laparoscopic nephrectomy.

CONFLICT OF INTEREST

None declared.

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