BJUI

Visceral obesity is a strong predictor of

perioperative outcome in patients undergoing
laparoscopic radical nephrectomy

BJU INTERNATIONAL

Masayuki Hagiwara, Akira Miyajima, Masanori Hasegawa,

Masahiro Jinzaki*, Eiji Kikuchi, Ken Nakagawa and Mototsugu Oya
Departments of Urology and *Diagnostic Radiology, Keio University School of Medicine, Tokyo, Japan
Accepted for publication 23 March 2012

Study Type Therapy (case series)

Level of Evidence 4

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

Whats 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.

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.

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
E980

RESULTS

CONCLUSIONS

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.

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.

patients are now being considered for

laparoscopic surgery.

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].

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 [68], and the criteria for
laparoscopic radical nephrectomy have now

KEYWORDS
nephrectomy, laparoscopy, visceral obesity,
metabolic syndrome, visceral fat area, renal
cell carcinoma, BMI

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

2 0 1 2 B J U I N T E R N A T I O N A L | 11 0 , E 9 8 0 E 9 8 4 | doi:10.1111/j.1464-410X.2012.11274.x

VISCERAL OBESITY PREDICTS COMPLEXITY OF LAPAROSCOPIC NEPHRECTOMY

FIG. 1. CT showing the degree of fat distribution. A,

Green area is the TFA. B, Green area is the VFA.
A

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

FIG. 2. Scatter plot showing the relationship

between BMI and operating time in laparoscopic
radical nephrectomy.
(ml) 400

Operating Time

350
300
250
200
150

r = 0.316
P < 0.001

100
50
15.0

20.0

25.0

30.0
BMI

35.0

40.0
(kg/m2)

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 [1115]. 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].

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.

2012 BJU INTERNATIONAL

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 [1820]. 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).
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

Pearsons 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; 95367)
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
25.029.9 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 nonvisceral 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.
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,
E981

HAGIWARA ET AL.

FIG. 3. Scatter plot showing the relationship

between VFA and operating time in laparoscopic
radical nephrectomy.

TABLE 1 Patient characteristics and demographics

90
31

VFA
VFA <100 cm2
56.1(12.0)
24
20

VFA 100 cm2

59.3 (12.2)

(ml) 400

0.172
<0.001

66
11
0.168

65
56

20
24

45
32

72
40
4
5

11
21
12
3.62 (1.67)
27
13
2
2
168.3 (42.6)

21
34
22
3.90 (1.67)
45
27
2
3
206.0 (57.2)

0.371
0.885

Characteristic
Age
<70 years
70 years
Gender
Male
Female
Laterality
Left
Right
Location
upper pole
middle pole
lower pole
Tumour size
<4.0 cm
4.0 cm
Clinical T category
T1a
T1b
T2a
T3a
BMI
<25 kg/m2
25 kg/m2
VFA
<100 cm2
100 cm2

E982

250
200
150

50
0

r = 0.348
P < 0.001
50

100

150

200
VFA

250

300

350
(cm2)

r = 0.348; Fig. 3), and the correlation

coefficient of VFA was higher than that of
BMI.

0.385

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).

0.374

DISCUSSION

<0.001

TABLE 2 Univariate and multivariate analyses of risk factors for prolonged operating time

No. of
patients

300

100

0.928
32
55
34

350
Operating Time

No. of
patients

Characteristic
Mean (SD) age
Gender
Male
Female
Laterality
Left
Right
Location
Upper pole
Middle pole
Lower pole
Mean (SD) tumour size, cm
Clinical T category
T1a
T1b
T2a
T3a
Operating time

Logistic regression analysis

Univariate
Multivariate
P
Hazard ratio (95% CI)
0.164

100
21
0.006

0.101

90
31
65
56
32
55
34
0.385
65
56
0.763
72
40
4
5
0.044

0.956

<0.001

0.009

87
34
44
77

3.70 (1.389.90)

Obesity is a common and growing problem

in industrialized countries [1], and it is
thought to be one of the risk factors for
RCC [2124]; 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.

2012 BJU INTERNATIONAL

VISCERAL OBESITY PREDICTS COMPLEXITY OF LAPAROSCOPIC NEPHRECTOMY

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
[2934]. 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
[3537].
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.

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.

10

11

CONFLICT OF INTEREST
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 [3841].
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

2012 BJU INTERNATIONAL

None declared.

12

REFERENCES
1

Popkin BM, Doak CM. The obesity

epidemic is a worldwide phenomenon.
Nutr Rev 1998; 56: 10614
Bhayani SB, Pavlovich CP, Strup SE
et al. Laparoscopic radical
prostatectomy: a multi-institutional
study of conversion to open surgery.
Urology 2004; 63: 99102
Mendoza D, Newman RC, Albala D
et al. Laparoscopic complications in
markedly obese urologic patients (a
multi-institutional review). Urology
1996; 48: 5627
Hagiwara M, Miyajima A, Matsumoto
K, Kikuchi E, Nakagawa K, Oya M.
Benefit of laparoscopic radical
nephrectomy in patients with a
high BMI. Jpn J Clin Oncol 2011; 41:
4004
Clayman RV, Kavoussi LR, Soper NJ

13

14

15

16

et al. Laparoscopic nephrectomy:

initial case report. J Urol 1991; 146:
27882
Janetschek G, Jeschke K, Peschel R,
Strohmeyer D, Henning K, Bartsch G.
Laparoscopic surgery for stage T1 renal
cell carcinoma: radical nephrectomy and
wedge resection. Eur Urol 2000; 38:
1318
Kerbl K, Clayman RV, McDougall EM
et al. Transperitoneal nephrectomy for
benign disease of the kidney: a
comparison of laparoscopic and open
surgical techniques. Urology 1994; 43:
60713
Rassweiler J, Fornara P, Weber M
et al. Laparoscopic nephrectomy: the
experience of the laparoscopy working
group of the German Urologic
Association. J Urol 1998; 160: 1821
Deane LA, Clayman RV. Laparoscopic
nephrectomy for renal cell cancer:
radical and total. BJU Int 2007; 99:
12517
Wilson BG, Deans GT, Kelly J, McCrory
D. Laparoscopic nephrectomy: initial
experience and cost implications. Br J
Urol 1995; 75: 27680
Anast JW, Stoller ML, Meng MV et al.
Differences in complications and
outcomes for obese patients undergoing
laparoscopic radical, partial or simple
nephrectomy. J Urol 2004; 172: 2287
91
Feder MT, Patel MB, Melman A,
Ghavamian R, Hoenig DM. Comparison
of open and laparoscopic nephrectomy
in obese and nonobese patients:
outcomes stratified by body mass index.
J Urol 2008; 180: 7983
Fugita OE, Chan DY, Roberts WW,
Kavoussi LR, Jarrett TW. Laparoscopic
radical nephrectomy in obese patients:
outcomes and technical considerations.
Urology 2004; 63: 24752; discussion
252
Gong EM, Orvieto MA, Lyon MB,
Lucioni A, Gerber GS, Shalhav AL.
Analysis of impact of body mass index
on outcomes of laparoscopic renal
surgery. Urology 2007; 69: 3843
Klingler HC, Remzi M, Janetschek G,
Marberger M. Benefits of laparoscopic
renal surgery are more pronounced in
patients with a high body mass index.
Eur Urol 2003; 43: 5227
Despres JP, Lemieux I. Abdominal
obesity and metabolic syndrome. Nature
2006; 444: 8817
E983

HAGIWARA ET AL.

17 Eckel RH, Grundy SM, Zimmet PZ. The

metabolic syndrome. Lancet 2005; 365:
141528
18 Kobayashi J, Tadokoro N, Watanabe
M, Shinomiya M. A novel method of
measuring intra-abdominal fat volume
using helical computed tomography. Int
J Obes Relat Metab Disord 2002; 26:
398402
19 Seidell JC, Oosterlee A, Thijssen MA
et al. Assessment of intra-abdominal
and subcutaneous abdominal fat:
relation between anthropometry and
computed tomography. Am J Clin Nutr
1987; 45: 713
20 Yoshizumi T, Nakamura T, Yamane M
et al. Abdominal fat: standardized
technique for measurement at CT.
Radiology 1999; 211: 2836
21 Bergstrom A, Pisani P, Tenet V, Wolk
A, Adami HO. Overweight as an
avoidable cause of cancer in Europe. Int
J Cancer 2001; 91: 42130
22 Renehan AG, Tyson M, Egger M, Heller
RF, Zwahlen M. Body-mass index and
incidence of cancer: a systematic review
and meta-analysis of prospective
observational studies. Lancet 2008; 371:
56978
23 Samanic C, Chow WH, Gridley G,
Jarvholm B, Fraumeni JF Jr. Relation of
body mass index to cancer risk in
362,552 Swedish men. Cancer Causes
Control 2006; 17: 9019
24 Setiawan VW, Stram DO, Nomura AM,
Kolonel LN, Henderson BE. Risk factors
for renal cell cancer: the multiethnic
cohort. Am J Epidemiol 2007; 166:
93240
25 Bray GA. Risks of obesity. Prim Care
2003; 30: 28199
26 Mokdad AH, Ford ES, Bowman BA
et al. Prevalence of obesity, diabetes,
and obesity-related health risk factors,
2001. JAMA 2003; 289: 769
27 Fasol R, Schindler M, Schumacher B
et al. The influence of obesity on
perioperative morbidity: retrospective
study of 502 aortocoronary bypass
operations. Thorac Cardiovasc Surg
1992; 40: 1269

E984

28 Jiganti JJ, Goldstein WM, Williams CS.

A comparison of the perioperative
morbidity in total joint arthroplasty in
the obese and nonobese patient. Clin
Orthop Relat Res 1993; 289: 1759
29 Despres JP, Moorjani S, Ferland M
et al. Adipose tissue distribution and
plasma lipoprotein levels in obese
women. Importance of intra-abdominal
fat. Arteriosclerosis. 1989; 9: 20310
30 Fujimoto WY, Newell-Morris LL, Grote
M, Bergstrom RW, Shuman WP.
Visceral fat obesity and morbidity:
NIDDM and atherogenic risk in Japanese
American men and women. Int J Obes
1991; 15 (Suppl. 2): 414
31 Fujioka S, Matsuzawa Y, Tokunaga K,
Tarui S. Contribution of intra-abdominal
fat accumulation to the impairment of
glucose and lipid metabolism in human
obesity. Metabolism 1987; 36: 549
32 Kanai H, Matsuzawa Y, Kotani K et al.
Close correlation of intra-abdominal fat
accumulation to hypertension in obese
women. Hypertension 1990; 16: 48490
33 Kobayashi H, Nakamura T, Miyaoka K
et al. Visceral fat accumulation
contributes to insulin resistance,
small-sized low-density lipoprotein, and
progression of coronary artery disease in
middle-aged non-obese Japanese men.
Jpn Circ J 2001; 65: 1939
34 Sparrow D, Borkan GA, Gerzof SG,
Wisniewski C, Silbert CK. Relationship
of fat distribution to glucose tolerance.
Results of computed tomography in
male participants of the Normative
Aging Study. Diabetes 1986; 35: 4115
35 New criteria for obesity disease in
Japan. Circ J 2002; 66: 98792
36 Despres JP, Lamarche B. Effects of diet
and physical activity on adiposity and
body fat distribution: implications for
the prevention of cardiovascular disease.
Nutr Res 1993; 6: 13759
37 Nakamura T, Tokunaga K, Shimomura
I et al. Contribution of visceral fat
accumulation to the development of
coronary artery disease in non-obese
men. Atherosclerosis 1994; 107: 23946
38 Weisberg SP, McCann D, Desai M,

39

40

41

42

43

44

45

46

Rosenbaum M, Leibel RL, Ferrante AW

Jr. Obesity is associated with
macrophage accumulation in adipose
tissue. J Clin Invest 2003; 112: 1796
808
Neels JG, Olefsky JM. Inflamed fat:
what starts the fire? J Clin Invest 2006;
116: 335
Trayhurn P, Wood IS. Adipokines:
inflammation and the pleiotropic role of
white adipose tissue. Br J Nutr 2004; 92:
34755
Alessi MC, Peiretti F, Morange P,
Henry M, Nalbone G, Juhan-Vague I.
Production of plasminogen activator
inhibitor 1 by human adipose tissue:
possible link between visceral fat
accumulation and vascular disease.
Diabetes 1997; 46: 8607
Hansson GK. Inflammation,
atherosclerosis, and coronary artery
disease. N Engl J Med 2005; 352:
168595
Hotamisligil GS. Inflammation and
metabolic disorders. Nature 2006; 444:
8607
Kosaka H, Yoshimoto T, Fujimoto J,
Nakanishi K. Interferon-gamma is a
therapeutic target molecule for
prevention of postoperative adhesion
formation. Nat Med 2008; 14: 43741
Hellebrekers BW, Kooistra T.
Pathogenesis of postoperative adhesion
formation. Br J Surg 2011; 98: 1503
16
Ljungberg B, Cowan NC, Hanbury DC
et al. EAU guidelines on renal cell
carcinoma: the 2010 update. Eur Urol
2010; 58: 398406

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
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.

2012 BJU INTERNATIONAL