Journal of Cancer Therapy, 2013, 4, 7-14
http://dx.doi.org/10.4236/jct.2013.49A2002 Published Online October 2013 (http://www.scirp.org/journal/jct)
7
Use of the American Society of Anesthesiologists
Classification as an Additional Planning Tool for Renal
Cell Carcinoma Assessment
Daniel Beltrame Ferreira1, Stênio de Cássio Zequi1, Walter Henriques da Costa1, Diego Abreu Clavijo2,
Ricardo Decia2, Deusdedit Cortez Neto1, Renato Rosa de Oliveira1, Gustavo Cardoso Guimarães1,
Ademar Lopes1
1Urology Division, Department of Pelvic Surgery, A. C. Camargo Cancer Center, Sao Paulo, Brazil; 2Department of Urology, Pasteur
Hospital, Montevideo, Uruguay.
Email: danielbeltrame@uol.com.br
Received July 24th, 2013; revised August 22nd, 2013; accepted August 31st, 2013
Copyright © 2013 Daniel Beltrame Ferreira et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ABSTRACT
Obje ctive: To determine the prognostic value of the American Society of Anesthesiologists (ASA) classification and of
the main clinical pathologic variables in renal cell carcinoma (RCC) patients who underwent surgical treatment. Me-
thods: In this international collaborative study, 376 RCC patients who underwent partial nephrectomy (PN) or radical
nephrectomy (RN) during the period 1989-2009 were assessed. The pathological data were reviewed by a single pa-
thologist, and all of the surgically treated patients had been previously evaluated by a team of anesthesiologists and
classified as ASA 1, ASA 2, or ASA 3. Results: In total, 318 patients were included in the study, with a mean follow-
up of 48 months. Incidental tumors represented 47% of the cases, while 11.6% presented with metastases at diagnosis.
Among the patients assessed, 38 (11.9%) were classified as ASA 1, 213 (67%) as ASA 2, and 67 (21.1%) as ASA 3. An
association between the ASA classification and the main clinicopathological variables of RCC was observed. The uni-
variate analysis for overall survival (OS) revealed significant differences in the survival curves according to the ASA
classification (p < 0.001). High-grade neoplasms, the presence of metastasis at diagnosis, clinical stage III/IV, and inci-
dental tumors remained as independent predictors of survival. Moreover, the multivariate analysis revealed a negative
impact of the ASA classification on OS (p = 0.001). Conclusions: The present study demonstrated a correlation be-
tween the ASA classification and the main prognostic factors of RCC and its impact on survival rates. ASA 3 patients
had more aggressive tumors, increased risk of perioperative complications, and worse outcomes compared with ASA1
or ASA 2. Thus, the ASA classification may be considered an additional tool for assessing and planning the treatment
of RCC patients.
Keywords: Comorbidity; Renal Cell Carcinoma; ASA; Prognosis; Oncology
1. Introduction
Renal cell carcinoma (RCC) accounts for 3% of malign-
nant neoplasms in adults, and its incidence has increased
over the last 20 years [1-3]. Although the incidental diag-
nosis is increasing worldwide, the mortality has not de-
creased [4]. The RCC evolution is unpredictable. Ap-
proximately 30% of patients present with metastases at
diagnosis, and approximately 40% of those individuals
treated for localized disease may experience recurrence
[5].
Most of the known prognostic factors are based on
clinicopathologic variables such as the stage, grade, his-
tologic type, and performance status (PS) [6,7]. The
presence of symptoms at diagnosis indicates larger tu-
mors that are more aggressive and have worse outcomes
[8]. The angiogenesis, apoptosis, and cell cycle biomar-
kers are underutilized in clinical practice and have a
prognostic potential that is not yet well established for
RCC [9]. The development of more accurate prognostic
factors is extremely important for individualized thera-
peutic planning [10-12].
RCC treatment with curative intent is primarily surgi-
cal. With increasing longevity and an aging population,
an increasing number of elderly RCC patients are candi-
Copyright © 2013 SciRes. JCT
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
8
dates for curative treatments, and their potential comor-
bidities should be considered [13]. Other patients, due to
their reduced life expectancy, are candidates for vigilant
observation protocols. Approximately 24% of RCC pa-
tients have at least two comorbidities that are relevant to
diagnosis [14].
Several evaluation and stratification mechanisms, such
as the Karnofsky’s Performance Status (KPS) [15], the
Eastern Cooperative Oncology Group (ECOG) [16], and
the Charlson comorbidity index [17], can be used to
evaluate this group of patients. However, these classifi-
cations assess the impact of cancer on the individual’s
general health, not considering the comorbidities and
their impact on the outcome of these tumors. It has been
recently reported that utilizing the American Society of
Anesthesiologists (ASA) classification has a prognostic
effect on survival rates and assessments of the metastatic
risk in RCC patients [18].
Moreover, the impact of these comorbidities in the
evolution of many tumors has been demonstrated, how-
ever, the prognostic value in RCC patients and the asso-
ciation with classical clinicopathologic variables are still
poorly studied [19,20].
Therefore, the aim of this investigation was to evaluate
the relevance and impact of classical clinicopathological
variables and the influence of comorbidities assessed by
the ASA classification on the survival rates of RCC pa-
tients who underwent surgical treatment in a South Ame-
rican collaborative study.
2. Material and Methods
In total, 376 consecutive patients from two South Ame-
rican centers were evaluated; the participants underwent
radical nephrectomy (RN) or partial nephrectomy (PN)
during the period from 1989 to 2009. The clinical data
were obtained from medical records of the AC Camargo
Hospital in São Paulo, Brazil, and from the Pasteur Hos-
pital in Montevideo, Uruguay. The pathological data
were reviewed and standardized by one experienced pa-
thologist. Patients who had other malignancies, who un-
derwent neoadjuvant treatment, who had incomplete
data, and who had missed follow-up were excluded
from the study, which featured a final sample of 318 pa-
tients. The investigation was approved by the Brazilian
National Committee for Ethics in Research (No. 549/
2011).
The ASA classification was performed preoperatively
by the anesthesiology staff, and the patients were classi-
fied as ASA 1, ASA 2 or ASA 3. Altogether, 77% of the
subjects underwent RN, and 23% underwent PN. The
mean age was 57.1 (14 - 86) years. Follow-up was con-
ducted every 3 months during the first 2 years, and there-
after, every 6 months. Metastasis assessment was per-
formed via computerized tomography or magnetic reso-
nance of the abdomen and pelvis and via chest radiogra-
phy or total-body bone scintigraphy.
The clinicopathological variables analyzed included
age, gender, tobacco use, presence of symptoms at diag-
nosis, type of surgery, stage (TNM, 2010) [21], Fuhr-
man grade, ECOG, KPS, histological subtype, vascular
and lymphatic invasion, presence of necrosis, lymph
node involvement, adrenal involvement, early and late
complications, follow-up period, and presence of meta-
stases. The correlation between the ASA classification
and the classical clinicopathological variables were eva-
luated.
The SPSS software for Windows, version 17.0 (SPSS
Inc., Chicago, USA), was used for the statistical analysis.
The comparison between the clinical and pathological
variables and the ASA classification was performed us-
ing the Pearson chi-square test. The variables with an ex-
pected frequency <5 were analyzed using Fisher’s exact
test.
Overall survival (OS) was defined as the time interval
between surgery and either the date of death or the last
visit. Cancer-specific survival (CSS) was defined as the
interval between surgery and either death from RCC or
the last visit. The study of overall and specific survival in
5 years was performed by the Kaplan-Meier method, and
the comparisons between the categories were performed
using the log rank test. For the multivariate analysis and
determination of variables with an impact on survival,
the Cox proportional hazards model (backward stepwise)
was used. The value of p < 0.05 was considered statisti-
cally significant.
3. Results
In total, 318 patients were evaluated with a mean follow-
up of 48 months. Among the population studied, the ma-
jority (60.3%) were male, 91% were white, and 107
(33.4%) were smokers. Incidental tumors accounted for
47% of cases, 37 patients (11.6%) exhibited metastases
at diagnosis, and clear cell carcinoma was the most com-
mon histological type found in 156 patients (74%).
Table 1 shows clinical and epidemiological features
and association with ASA classification of all patients.
Thirty-eight patients (11.9%) were classified as ASA 1,
213 (67%) patients as ASA 2, and 67 (21.1%) patients as
ASA 3. The ASA 3 patients were older than the ASA 1
and ASA 2 patients, with approximately 73% of ASA 3
patients in the range of 60 to 82 years of age. Metastases
at diagnosis occurred in 23.9% of the ASA 3 patients,
versus 10% (21 of 213) the ASA 2 patients. No ASA 1
patients had metastatic disease at diagnosis. The ASA 3
patients had 25% of the early complications and 18.8%
of the late complications. Tab le 2 shows pathological
Copyright © 2013 SciRes. JCT
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
Copyright © 2013 SciRes. JCT
9
Table 1. Clinical and epidemiological characteristics and association with ASA classification.
Variable ASA 1 ASA 2 ASA 3 P value
n (% within ASA) n (% within ASA) n (%within ASA)
Gender
Male 24 (63.2) 125 (58.7) 42 (62.7)
Female 14 (36.8) 88 (41.3) 25 (37.3) 0.774
Smoking
No 20 (64.5) 108 (57.8) 41 (70.7)
Yes 11 (35.5) 79 (42.2) 17 (29.3) 0.194
ECOG(PS)
0 31 (100) 105 (78.9) 7 (14.6)
1 + 2 0 (0) 28 (21.1) 41 (85.4) 0.001
KPS
<80 0 (0) 2 (1.5) 11 (22.9)
80 31 (100) 130 (98.5) 37 (77.1) <0.001
Metastasis
No 38 (100) 192 (90.1) 51 (76.1)
Yes 0 (0) 21 (9.9) 16 (23.9) 0.001
Transfusion
No 27 (87.1) 106 (79.7) 35 (72.9)
Yes 4 (12.9) 27 (20.3) 13 (27.1) 0.309
Clinical stage
I/II 28 (77.8) 129 (62.3) 37 (56.1)
III/IV 8 (22.2) 78 (37.7) 29 (43.9) 0.041
Age
23 - 44 years 6 (35.3) 14 (19.7) 0 (0)
45 - 59 years 14 (58.8) 39 (54.9) 6 (27.3)
60 - 82 years 1 (5.9) 18 (25.4) 16 (72.7) <0.001
Symptomatic diagnosis
No 19 (51.4) 103 (48.8) 26 (39.4)
Yes 18 (48.6) 108 (51.2) 40 (60.6) 0.352
Early complicatons
No 28 (90.3) 119 (89.5) 36 (75)
Yes 3 (9.7) 14 (10.5) 12 (25) 0.034
Late complications
No 29 (93.5) 123 (92.5) 39 (81.3)
Yes 2 (6.5) 10 (7.5) 9 (18.8) 0.043
ECOG (PS), Eastern Cooperative Oncology Group Performance Staus; KPS, Karnofsky Performance Status.
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
10
Table 2. Pathological characteristics and association with ASA classification.
Variable ASA 1 ASA 2 ASA 3 P value
n (% within ASA) n (% within ASA) n (%within ASA)
Fat/Sinus invasion
No 31 (81.7) 162 (76.4) 43 (64.2)
Yes 7 (18.4) 50 (23.6) 24 (35.8) 0.029
Tumor size
<7 cm 19 (65.5) 89 (68.5) 24 (51.1)
>7 cm 10 (34.5) 41 (46.7) 23 (48.9) 0.102
Lymph node invasion
No 28 (96.6) 118 (90.8) 42 (89.4)
Yes 1 (3.4) 12 (9.2) 5 (10.6) 0.530
Fuhrman grade
Low (I/II) 27 (71.1) 143 (69.8) 33 (50.8)
High (III/IV) 11 (28.9) 62 (30.2) 32 (49.2) 0.015
MVI
No 27 (87.1) 103 (78) 38 (79.2)
Yes 4 (12.9) 29 (22) 10 (20.8) 0.527
Necrosis
No 23 (60.5) 123 (58.3) 29 (43.3)
Yes 15 (39.5) 88 (41.7) 38 (56.7) 0.046
Adrenal
No 38 (100) 200 (94.3) 64 (95.5)
Yes 0 (0) 12 (5.7) 3 (4.5) 0.316
Clear cell histology
No 12 (38.7) 36 (27.5) 7 (14.6)
Yes 19 (61.3) 95 (72.5) 41 (85.4) 0.050
MVI: microvascular invasion.
characteristics and association with ASA classification.
An association was found between the ASA classifica-
tion and the ECOG, KPS, metastasis at diagnosis, perire-
nal fat invasion, clinical stage, Fuhrman grade, presence
of necrosis, age at onset, and rate of early or late compli-
cations.
The OS and CSS rate at 5 years for all patients was
74.1% and 81%, respectively. At the final follow-up, 76
patients had died, including 56 (73.6%) who died from
RCC. In the univariate analysis, the rates of OS for ASA
1, ASA 2, and ASA 3 were 88.2%, 77.6%, and 54.2%,
respectively (p < 0.001). The CSS at 5 years for ASA 1,
ASA 2, and ASA 3 was 88.2%, 83.1%, and 69.5%, re-
spectively (p = 0.009) (Figure 1). When considering
only ASA 1 and ASA 2 patients, no statistically signifi-
cant differences existed in the curves for OS (p = 0.216)
and CSS (p = 0.505). The risk of overall death in the
ASA 3 patients was 2.82 times greater than in the ASA 1
or ASA 2 patients (p = 0.001; 95% IC 1.7 - 4.53). Di-
sease recurrence occurred in 45 patients, with no diffe-
rence between the disease-free survival (DFS) curves
stratified by ASA classification (p = 0.483).
After multivariate analysis for OS and CSS, the inci-
dental tumors, presence of metastasis at diagnosis, Fuhr-
man grade, and clinical staging were considered statisti-
cally significant independent factors for survival. Fur-
Copyright © 2013 SciRes. JCT
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
11
thermore, the ASA classification also had a predictive
impact on the OS (p = 0.010) (Table 3).
The survival curve analysis stratified by ASA was also
performed after the exclusion of 37 cases with metastases
at diagnosis. Of the 281 cases of tumors without meta-
stases, death by cancer occurred in 34 patients (12%).
Death from other causes in patients with non-metastatic
disease occurred in 19 patients (6.7%). The CSS at 5
years for ASA 1, ASA 2, and ASA 3 was 88.2%, 87.4%,
and 83.7%, respectively (p = 0.646). An effect of ASA
on the OS at 5 years after the exclusion of metastatic
cases (p = 0.030) was also observed. At the final follow-
up, 88.2% of the ASA 1 patients, 81.9% of the ASA 2
patients, and 62.8% of the ASA 3 patients were still
alive.
4. Discussion
The evaluation and prognosis of RCC patients are based
on clinicopathological variables that are recognized by
their capacity to predict survival, recurrence, and disease
progression [22]. However, these prognostic factors alone
cannot accurately differentiate tumors of low malignant
potential from clinically relevant tumors. Thus, with an
aging population and the gradual increase in chronic di-
seases, interest in the study of the prognostic value of co-
morbidities in patients with various tumors has increased
[23].
The ASA classification has been widely employed to
assess the risk of perioperative complications based on
comorbidities [24]; however, use of the classification as a
prognostic factor in cancer patients is still controversial
[25]. In a retrospective study of more than 500 patients
with urothelial bladder carcinoma who were subjected to
cystectomy, Mayr et al. demonstrated the impact of co-
morbidities assessed by the ASA classification on the
cancer-specific mortality [26].
In a recent study from our group, Zequi et al. evalu-
ated the ASA classification as a prognostic factor in 141
RCC patients subjected to surgical treatment. In that stu-
dy, ASA-stratified patients exhibited effects on the OS,
CSS, and DFS rates, as well as on the risk of developing
metastases. The investigation also revealed that ASA-3
patients had fewer incidental tumors at diagnosis, thereby
representing a group with high risks of death and disease
progression compared with ASA 1 and 2 [18].
The present study confirmed the ASA classification’s
impact on the OS of RCC patients after univariate and
multivariate analysis. At the final follow-up, 45.7% of
the ASA 3 patients, 22.3% of the ASA 2 patients, and
only 11.7% of the ASA 1 patients had died. Considering
only the 20 cases of non-oncological death, 11 patients
(55%) were ASA 2, and nine patients (45%) were ASA 3.
Thus, the risk of death from other causes was approxi-
mately 4 times higher in the ASA 3 patients compared
with the ASA 2 patients (p = 0.002). These findings
demonstrate the importance and effect of comorbidities
assessed by the ASA in the prognosis of patients sub-
jected to surgical treatment for RCC. Moreover, it is not
known whether the presence of several comorbidities
affects the immune system of RCC patients, resulting in
more biologically aggressive disease.
The risk of death from other causes in patients with
localized RCC was recently evaluated by Chang et al.
[27]. In their study, factors such as advanced age, low
(a) (b)
Figure 1. Overall survival (OS) and disease specific survival (DSS) according ASA classification. (a) 5-year OS curves; (p <
0.001); (b) 5-year CSS curves (p = 0.003).
Copyright © 2013 SciRes. JCT
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
12
Table 3. Cox regression analysis for overall survival (OS) and disease-specif ic surviva l (DSS).
Feature 5-year OS 5-year DSS
Univariate Multivariate Univariate Multivariate
HR P value HR (95% CI) P valueHR P valueHR (95% CI) P value
ASA score <0.001 0.010 0.040 0.894
1 1.0 (Reference) 1.0 (Reference) 1.0 (Reference) 1.0 (Reference)
2 1.858 2.195 (0.296 - 16.858) 1.416 0.693 (0.096 - 5.002)
3 4.907 8.650 (1.052 - 71.148) 3.121 1.186 (0.097 - 14.468)
MVI 3.661 <0.001 1.956 (0.740 - 5.170)0.1765.172<0.0011.868 (0.646 - 5.399)0.249
Necrosis 2.502 <0.001 1.864 (0.799 - 4.344)0.1494.107<0.0011.082 (0.336 - 3.487)0.895
Adrenal 2.309 0.035 1.123 (0.181 - 6.982)0.9013.2650.003 0.566 (0.138 - 2.314)0.428
Metastasis 6.594 <0.001 2.780 (1.048 - 7.377)0.0408.961<0.0014.686 (1.809 - 12.103)0.001
Renal vein invasion 2.198 0.006 0.642 (0.237 - 1.737)0.3832.737<0.0010.479 (0.167 - 1.374)0.171
Fat/Sinus invasion 2.282 <0.001 0.556 (0.212 - 1.461)0.2343.250<0.0010.799 (0.238 - 2.682)0.717
Lymph nodes invasion 6.257 <0.001 1.223 (0.446 - 3.353)0.6958.130<0.0011.723 (0.446 - 6.660)0.430
Symptomatic vs Incidental tumors 3.582 <0.001 2.989 (1.108 - 8.066)0.0315.294<0.0013.495 (1.007 - 12.128)0.049
ECOG PS (1 + 2 vs 0) 2.527 0.002 0.913 (0.269 - 3.097)0.8842.3560.009 1.071 (0.330 - 3.480)0.640
KPS (<80 vs 80) 3.122 0.010 0.665 (0.160 - 2.767)0.6392.3570.105 1.407 (0.207 - 9.557)0.727
Tumor size (>7 cm vs <7 cm) 6.086 <0.001 1.086 (0.379 - 3.116)0.87810.590<0.0012.088 (0.637 - 6.846)0.224
Clinical stage (III/IV vs I/II) 3.481 <0.001 5.374 (1.967 - 14.681)0.0016.499<0.0018.710 (1.863 - 40.718)0.006
Fuhrman grade (high vs low) 3.202 <0.001 3.298 (1.546 - 7.033)0.0024.189<0.0012.837 (1.107 - 7.270)0.030
HR, hazard ratio; CI, confidence interval; MVI, microvascular invasion.
body mass index, and an ASA score of 3 to 4 were inde-
pendent predictors of non-cancer-related death. Berdijis
et al. [28] evaluated 1,023 patients subjected to surgical
treatment for RCC and demonstrated that the morbidity
and mortality did not increase with age; however, there
was a positive correlation with the ASA classification. In
an epidemiologic study of almost 1400 RCC patients,
hypertension and diabetes were present in 58% and 17%
of the patients, respectively [29]. Thus, the presence of
comorbidities assessed by the ASA classification is asso-
ciated with increased morbidity and mortality during
RCC treatment and may influence the therapy. Our re-
sults revealed that the percentage of perioperative com-
plications in the ASA 1, ASA 2, and ASA 3 patients was
16.1%, 15.8%, and 29.2%, respectively. The risk of early
or late complications in the ASA 3 patients was at least
double that of the ASA or ASA 2 patients, combined
(odds ratio, 2.18; p = 0.038).
Further results demonstrated an association between
the ASA classification and the main clinicopathological
variables, contrary to the findings of Han et al. [30]. Of
the ASA 3 patients in the present study, 23.9% had meta-
stases at diagnosis, which was a risk 2.86 times greater
than in the ASA 2 patients (p = 0.003). None of the ASA
1 patients exhibited metastatic disease. Furthermore,
among the ASA 3 patients, nearly one-half had high-
grade disease. Perirenal fat invasion, advanced clinical
stage, age, presence of necrosis, and measures of PS
(such as ECOG and KPS) were also associated with a
higher ASA classification. Approximately 23% of the
ASA 3 patients had KPS < 80, and all of the ASA 1 pa-
tients were classified as ECOG 0. Thus, considering the
whole sample, the patients stratified as ASA 3 had disea-
se with more criteria of aggressiveness and an important
impact on PS scales such as KPS and ECOG.
By contrast, after the exclusion of cases with metasta-
sis at diagnosis, no association was observed between the
main tumor-dependent variables and the ASA stratifica-
tion, thus characterizing the aggressiveness of tumors
that presented with metastatic disease. However, in this
group of patients, the ASA stratification was associated
with patient-dependent variables such as the ECOG, KPS,
and age. Patients with metastases rapidly progress to
death and should be treated more aggressively. However,
Copyright © 2013 SciRes. JCT
Use of the American Society of Anesthesiologists Classification as an Additional Planning Tool
for Renal Cell Carcinoma Assessment
13
if the patient has a high number of comorbidities, then
the validity of this approach might be reconsidered.
An important application of evaluating the ASA clas-
sification might involve non-metastatic patients, patients
with small renal masses, elderly individuals, or those
with multiple comorbidities. Whereas ASA 3 patients
exhibit shorter survivals, higher risk of death from other
causes, and increased risk of perioperative complications,
perhaps this group of patients could be spared from the
more aggressive treatments.
In addition to the ASA classification, prognostic fac-
tors such as the Fuhrman grade, presence of metastasis at
diagnosis, clinical stage, and incidental tumors remained
as independent predictive variables of OS and CSS.
Our study is limited by its retrospective nature and its
being composed of a historic series from two institutions
over a long period. Moreover, the ASA classification has
a subjective aspect; however, it is time honored, is easily
memorized, and has the advantage of being prescribed by
another professional, thereby avoiding surgeon bias. In
addition, this classification is already routinely available
within medical records (requiring no additional develop-
ment costs), is recognized worldwide, and allows for the
scientific standardization of information.
The present study demonstrated the negative impact of
the ASA classification on survival rates and its associa-
tion with the main RCC prognostic variables. It is estab-
lished that RCC management should be performed indi-
vidually, considering the patient’s life expectancy, asso-
ciated risks, and comorbidities. Thus, the ASA classifica-
tion may be used as an additional tool for assessing and
planning the treatment of RCC patients, based on its cli-
nical applicability, easy access during the preoperative
routine, and high reproducibility.
5. Conclusion
The present study demonstrated the value and impact of
the ASA classification as an independent predictor of OS
in RCC patients who underwent surgical treatment and
revealed the association between the ASA classification
and the major prognostic variables. Based on these find-
ings, the ASA classification may also be employed as an
additional predictive tool for managing RCC patients
with limited life expectancies or patients with multiple
comorbidities. Furthermore, the ASA classification may
facilitate the evaluation of candidates for active surveil-
lance protocols or minimally invasive treatments, as an
addition to the already established prognostic factors.
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