Venous Compliance in Trained Females
39
Journal of Exercise Physiologyonline
(JEPonline)
Volume 12 Number 4 August 2009
Managing Editor
Tommy Boone, PhD, MPH
Editor-in-Chief
Jon K. Linderman, PhD
Review Board
Todd Astorino, PhD
Julien Baker, PhD
Tommy Boone, PhD
Larry Birnbaum, PhD
Eric Goulet, PhD
Robert Gotshall, PhD
M. Knight-Maloney, PhD
Len Kravitz, PhD
James Laskin, PhD
Derek Marks, PhD
Cristine Mermier, PhD
Chantal Vella, PhD
Ben Zhou, PhD
Official
Research Journal of
the American Society of
Exercise Physiologists
(ASEP)
ISSN 1097-975
Sports Physiology
Calf Venous Compliance in Endurance Trained Females
JULIANE P. HERNANDEZ, BETSY E. GODAR
Department of Kinesiology, Southern Illinois University, Carbondale, Illinois
ABSTRACT
Hernandez, JP, Godar, BE. Calf Venous Compliance in Endurance
Trained Females. JEPonline 2009;12(4):39-49. Endurance training has
been shown to increase calf venous compliance in males, but the effects
of endurance training on calf venous compliance in females have yet to
be established. The purpose of this investigation was to determine the
effects of endurance training status on the calf venous compliance in
young females. Twenty healthy endurance trained collegiate track and
cross country athletes [10 female (20.50.4 yrs, 59.41.6 ml*kg-1*min-1)
and 10 males (22.91.3 yrs, 64.3 2.8 ml*kg-1*min-1)], and twenty
healthy average [10 female (21.70.5 yrs, 35.91.8 ml*kg-1*min-1) and
10 male (23.71.0 yrs, 42.61.8 ml*kg-1*min-1)] volunteers underwent
maximal graded exercise tests and assessment of calf venous
compliance. Utilizing venous occlusion plethysmography, calf venous
compliance was determined in both groups using the first derivative of
the pressure-volume relation during cuff pressure reduction. Venous
capacitance and capillary filtration volumes were determined following
cuff pressure inflation. VO2max was significantly greater in the
endurance trained females and males compared to the average-fit
females and males (p<0.05). The endurance trained females had higher
calf venous compliance than the average fit females (p<0.05; ~40%;
0.0022 vs 0.0013 ml 100ml-1 mmHg-1), and the endurance trained
females had significantly greater capillary filtration volumes than both of
the average fit groups and the endurance trained males (p<.05).
Endurance trained females have greater calf venous compliance than
females of average fitness.
Key Words: Peripheral Circulation, Training, Gender, Blood Flow.
Venous Compliance in Trained Females
40
INTRODUCTION
The venous vasculature is a volume reservoir containing approximately 70% of our total blood
volume. This system is designed to preserve flow of blood from the tissues to the heart during
cardiovascular stress. Variations in blood volume can be overcome by altering the total capacity of
the venous system to maintain pressure, thus ensuring venous return to the heart (1,2). This
pressure-volume relationship is an important part of cardiovascular homeostasis. Veins are 30-50
times more compliant than arteries and in the upright posture 70% of the blood volume falls below the
level of the heart. This translocation of blood away from the heart causes a stress to the
cardiovascular system that is counter-regulated by sympathetic modulation, specifically higher
peripheral resistance and increases in heart rate as well as activation of the skeletal muscle pump (2,
3).
Endurance trained male athletes have consistently higher venous compliance in the calf than their
more sedentary peers (4,5). However, this training affect has not been directly assessed in females
and recent research suggests that calf venous compliance in untrained females is lower than that of
untrained males (6,7). Females are more prone to orthostatic intolerance than males (8,9, 10, 11)
and female runners appear to be more susceptible to hypovolemic intolerance than non runners (12).
Therefore the primary purpose of this investigation was to determine the calf venous compliance in
endurance trained females compared to their counterparts of average fitness. We hypothesized that
calf venous compliance would be significantly higher in the endurance trained than in the normally
active females.
METHODS
Participants
Twenty healthy endurance-trained track and cross-country athletes (10 female and 10 male) were
recruited from a Division I University along with twenty (10 female and 10 male) volunteers of average
fitness from the university. The endurance trained athletes were matched as closely as possible for
training volume and VO2max. The average fit participants reported no regular physical activity
defined as exercising 20-45 minutes 3 times per week. All participants were healthy based on
medical history, resting blood pressure < 140/90 mmHg, no reported use of tobacco, body fat
percentage < 35%, free of any diagnosed cardiovascular disease and not taking any cardiovascular
medication. There was no known venous insufficiency and participants refrained from caffeine
ingestion for 12 hours and food consumption for 1 hour before testing. Data collection was performed
at a stable room temperature between 23-25°C. Female participants were tested in the follicular
phase (3-10 days from the first day of menstruation) of their menstrual cycle, and all reported regular
menstrual cycles. Written informed consent was obtained according to practices established by the
Southern Illinois University Human Subjects Committee.
Experimental Procedures
A balance scale and stadiometer were used to assess body mass (kg) and height (cm). Body
composition was estimated by a 3-site protocol using Lange Skinfold Calipers. Maximal oxygen
consumption was measured during graded treadmill exercise to exhaustion using open-circuit
spirometry (TrueMax 2400 ParvoMedics). Standard criteria for achievement of valid maximum
oxygen consumption was met in all participants (13). Strain gauge plethysmography (ECR5
Hokanson, Bellevue, WA) was used to assess changes in calf volume and a venous collecting cuff
was used to control pressure (AG101 Hokanson, Bellvue, WA). Blood pressure and heart rate were
continuously monitored by Dinamap (J & J Medical, Tampa, FL) non-invasive blood pressure monitor.
Venous Compliance in Trained Females
41
Experimental Protocol
The methods selected for the present study were similar to those used previously by Hernandez and
Franke (2004), a slightly modified version of the procedures validated by Halliwill et al. (1999).
Participants reported to the laboratory on two separate occasions. The first visit was to obtain
anthropometric data and perform a VO2 max test to determine fitness level. Using the formula r2L,
calf volume was calculated from four girth measures obtained equidistantly between the medial
malleolus and the tibial plateau and one calf segment length. Venous compliance measurements
were conducted on the second visit, which was at least 48 hours after the treadmill test. Changes in
calf volume were assessed non-invasively using strain gauge plethysomography. With the participant
in a supine position the right leg was elevated above heart level and supported at the ankle and thigh
to promote venous drainage. A venous collecting cuff was applied proximal to the right knee and
connected to an external air source that allowed pressure to be precisely and rapidly modulated
within the cuff. A mercury in-silastic strain gauge was placed around the maximal circumference of
the calf. After instrumentation and 30 minutes rest, venous collecting cuff pressure was applied at 60
mmHg for 8 minutes and subsequently reduced by 5mmHg /5s to 10 mmHg. At the onset of cuff
pressure, an initial rapid increase in the volume of the calf occurred which is associated with the
capacitance response (16) followed by a slower, but continuous rise in volume caused by net
transcapillary fluid filtration from blood to tissue as described by Schnizer and colleagues (1978, 17).
During cuff pressure reduction (5mmHg/5 seconds) volume declined rapidly (Figure 1).
Data Analysis
All data were recorded on a Dell PC (Biopac data acquisition software) for analysis. Resulting
pressure-volume curves during the step down in pressure are described by the quadratic regression
equation [( limb volume) = 0 + 1(cuff pressure) + 2(cuff pressure)]. The group-average
regression parameters 1 and 2 were used together as an estimate of compliance [compliance = 1 +
22(cuff pressure)]. The first derivative yields a linear pressure-compliance relationship and this
slope was used to determine training (endurance vs. average fit) and sex (females vs. males)
differences.
The capacitance response was calculated from the volume increase at the onset of cuff pressure to
the line defined from the filtration slope between 3 and 8 minutes of cuff pressure application. Total
capillary filtration during cuff pressure was calculated from the rate of filtration (ml/min) times the time
of the cuff pressure application (8 min). Total calf volume increase was the sum of the capacitance
and net capillary filtration volumes.
Differences in participant characteristics, compliance regression parameters, capacitance, and
capillary filtration volumes were determined using two-way ANOVA (fitness X gender). Statistical
significance was set at p<.05. When significance was revealed by the ANOVA, group differences
were located using the Student Newman-Keuls post hoc test.
RESULTS
Participant Characteristics
Physical characteristics are summarized in Table 1. VO2max was significantly greater in the
endurance trained groups compared to the sedentary groups (p<.05). Both average fit groups and
the endurance trained males had a greater body mass than the endurance trained females (p<.05).
The average fit females had a greater body fat percentage than all other groups and the endurance
trained males had a lower body fat percentage than all other groups (p<.05). Body mass index was
greater in the average fit groups than the endurance trained groups (p<.05). The average males had
higher systolic blood pressure than all the other groups and a higher resting heart rate than the
endurance trained males (p<.05). Height was greater in the males of both average and endurance
Venous Compliance in Trained Females
42
trained groups than the females (p<.05), and calf volume was significantly lower in the endurance
trained
Table 1. Selected Participant Characteristics.
females than
Variables
Average Fit Average Fit
Endurance
Endurance
all
other
Female
Male
Trained
Trained
groups
Female
Male
(p<.05).
21.7±1.7
23.7±3.2
20.5±1.4
22.9±3.9
Age (yr)
164.9±6.0bd 174.5±4.7
167±5.2bd
179.2±4.3
Height (cm)
c
c
75.3±12.5
85.7±16.0
58.6±8.2
72.8±6.6c
Body Mass (kg)
ac
a
29.8±3.6
17.7±5.3
16.5±2.8
12.0±4.8abc
Bodyfat (%)
27.6±3.6
28.1±4.6
20.9±2.1ab
22.7±2.0ab
BMI
acd
122.1±11.6 127.1±11.0
111.5±8.8
117.6±7.3
Systolic BP (mmHg)
85.0±8.8c
89.4±8.4c
70.2±9.4
76.8±6.1b
Diastolic BP (mmHg)
76.7±6.8d
67.4±10.5
61.7±6.2
Resting Heart Rate (bpm) 68.0±7.6
3725.1±560 3912.2±523
3106.2±381abd 3608.3±309
Calf volume (ml)
VO2max (ml*kg-1*min-1)
35.8±5.6
42.5±5.8
59.4±5.1ab
64.3±9.0ab
Values are means  SD; n = 40 (10 in each group). VO2max, maximal oxygen
consumption; BP, blood pressure; BMI, body mass index. ap< 0.05 vs. average
females; bp< 0.05 vs. average males. cp<0.05 vs. endurance trained female.
d
p<0.05 vs. endurance trained male.
Calf Venous
Compliance
Table
2
displays
the
regression
parameters 0,
1, and 2
calculated
(means  SD)
for
average
and endurance
trained
females and males. In both average groups, pressure-volume curves derived from the calf were less
steep than in the endurance trained groups (p<.05; Table 2 and Figure 2). The pressure-volume and
compliance-pressure curves illustrate these differences in Figures 2 and 3. Calf venous compliance
was lower in the average fit groups than the endurance trained participants (Figures 3 & 4).
Endurance trained females were ~40% more compliant than average females (p<.05; 0.0022 vs
0.0013 ml 100ml-1 mmHg-1) and endurance trained males had ~50% greater compliance than
average males (p<.05; 0.0025 vs 0.0012 ml 100ml-1 mmHg-1; Figures 3 & 4). Calf venous compliance
differences were quantified using the slope of the compliance-pressure line. Calf venous compliance
between the females and males did not differ significantly in either fitness group (Figure 3 & 4).
When training differences were quantified by calculating percent change in β1 at an intravenous
pressure of 0 mmHg (5) the endurance trained females were ~35% more compliant than the average
females and the endurance trained males were ~ 47% more compliant than the average males
(p<.05). Two methods of quantifying compliance were used in order to compare the present findings
with previous research (5) that used different methods of quantifying compliance differences.
The endurance trained females and males had greater capacitance responses than did the average
fit
groups
(p<.05; Figure Table 2. Pressure-Volume Regression Parameters.
β0
β1
β2
5).
0.9559±.4971
0.0797±.0223cd -.0007±.0002cd
Average Female
Interestingly,
1.1415±.7469
.0751±.0286cd
-.0006±.0003cd
the endurance Average Male
abd
2.3544±1.1253
.1230±.0229
-.0011±.0003
Endurance Trained Female
trained
Endurance
Trained
Male
1.3434±.8413
.1428±.0264
-.0012±.0002
females
had
Values are means + SE. Δ Calf Volume = β0 + β1 *(cuff pressure) + β2 *(cuff
significantly
pressure)2; ap< 0.05 vs. average females; bp< 0.05 vs. average males. cp<0.05 vs.
greater
endurance trained female. dp<0.05 vs. endurance trained male.
capillary
filtration volumes than both of the average groups and the endurance trained males (p<.05; Figure 5).
There was no difference between males and females in capacitance volumes in either the average
groups or the endurance trained groups. Total calf volume increase was greater in the endurance
trained groups than the average fit group (p<.05; Figure 5), but not different between the sexes in
either group.
Venous Compliance in Trained Females
43
DISCUSSION
Chang in Volume (ml/dl)
Pressure (mmHg)
To the best of our knowledge this is the first study to investigate differences in lower limb venous
compliance between endurance trained female athletes and females of average fitness. Based on
previous findings in males (4,14), we
60
hypothesized that calf venous compliance would
be higher in the endurance trained than in the
normally active females. The main findings of the
study support this hypothesis showing that
endurance trained females have significantly
0
greater venous compliance, capacitance volume,
and net capillary filtration volumes than their
average fit peers.
This is consistent with
previous research conducted primarily in males
6
(4,14,18). Interestingly, we did not find a gender
difference in calf venous compliance in either the
endurance trained or the average fit group. This
is in direct contrast to earlier investigations (6, 7).
We did however find that the endurance trained
0
females had significantly greater capillary
filtration volumes than either of the male groups
0
3
6
9
and the average fit females.
Time (min)
Figure 1. Original tracing showing calf volume
Figure 1.in response to 60 mmHg cuff pressure
changes
applied to the thigh for 8 minutes and subsequent
reduction in pressure of 5 mmHg/5 seconds in a
21 year old endurance trained male.
Endurance Training
The finding of increased calf venous compliance
in endurance trained females compared to their
normally active peers supports Monahan and
colleagues (2001) and Hernandez and Franke
(2005), showing endurance training is associated with higher calf venous compliance in males.
Monahan and colleagues (2001) found a significant positive correlation between calf venous
compliance and maximal oxygen consumption in a group of sedentary and trained older and young
men (r = 0.07). However, in a previous investigation, we did not find as strong a correlation between
calf venous compliance and maximal oxygen consumption (r = 0.297) despite significantly higher calf
venous compliance in the trained groups. Our previous investigation included females in the groups
of older and younger, trained and sedentary individuals, and it was initially speculated that the
females may have affected the relationship between fitness and compliance, but when separated for
gender, there was inadequate statistical power (5).
To the best of our knowledge, this is the first study to show the capacitance and capillary filtration
volumes in endurance trained and normally active men and women using the pressure reduction
method of non-invasively assessing compliance (17). Total calf volume increase was greater in the
endurance trained females than their normally active counterparts (p<.05). The capacitance
response of the endurance trained athletes was almost twice as much as the volumes seen in the
normally active individuals. The capillary filtration volumes were greater in the female athletes than
the female normally active participants while there was no difference in the capillary fitration volume
with endurance training in men. The capacitance response in the athletes is most likely being driven
by the higher compliance of the vasculature as well as higher blood volumes and greater
capillarization (2). Lindenberger and Lanne (2007) found that application of lower body negative
pressure (LBNP; 11, 22 & 44 mmHg) yielded increases in capillary filtration volumes with higher
Venous Compliance in Trained Females
44
pressures in men and women. Further, they found that the women had higher capillary fitration
volumes than the men at the lower LBNP . The fact that our cuff pressure application (60 mmHg)
was the same for all groups indicates a possible differential response in the vasculature of females to
training. The participants assessed by Lindenberger and Lanne (2007) were described as healthy
and of average fitness, but they may have been slightly more fit than the average fit group used in the
current investigation. Lindenberger and Lanne (2007) reported a mean resting heart rate of 61 (2)
beats per minute and a resting systolic blood pressure of 107(1) mmHg, while the average fit females
in the current investigation had a mean resting heart rate of 68(2) beats per minute and a systolic
blood pressure of 122 (4) mmHg. The gender difference in the capillary filtration volumes will be
discussed in the next section (18).
A.
B.
Compliance (ml/dl/mmHg)
Volume (ml/dl)
Possible
mechanisms
for
7
7
alterations in calf venous
6
6
compliance are quite similar to
5
5
those
on
arterial
central
4
4
compliance.
Compliance of
3
3
veins appears to decline with
age and improve with chronic
2
2
physical activity comparable to
1
1
central arterial compliance (19).
0
0
0
10
20
30
40
50
60
0
10
20
30
40
50
60
Mechanistic speculations on
0.16
0.16
changes in venous compliance
0.14
0.14
Average Female
Average Male
have focused on alterations in
Endurance
Endurance Trained
0.12
0.12
Trained
Female
Male
the ratio of elastin to collagen in
0.1
0.1
the vessel wall or changes in
0.08
0.08
the vessel composition caused
0.06
0.06
by alterations in sympathetically
0.04
0.04
meditated vascular quality (6, 7,
0.02
0.02
18).
Halliwill et al. (1999)
0
0
0
10
20
30
40
50
60
0
10
20
30
40
50
60
demonstrated
sympathetic
Pressure (mmHg)
Pressure (mmHg)
stimulation did not affect Figure
Figure 2.
2. Volume-Pressure curves (top) and Volume-Compliance
venous compliance, suggesting Slopes (bottom) for A. Average fit and endurance trained females
venous vasculature compliance (red) and B. Average fit and endurance trained males (blue).
is increased by alterations in Means + SD. The endurance trained groups had significantly
the composition of the vessel steeper compliance slopes than the average fit groups (p<.05) as
wall. In contrast, Monahan and shown in Table 2.
Ray (2004) showed that
sympathoexcitation reduced venous compliance, but only in men. Hernandez and Franke (2004)
found no changes in calf venous compliance in an older population after 3 months of endurance
training, but reported an improvement after 6 months that wasn’t significant but probably meaningful
(p = .07), implying alterations may take time to occur supporting the idea of vessel wall remodeling.
Further research exploring the mechanisms responsible for increasing venous compliance with
endurance training is still warranted.
Gender Differences
Monahan and Ray (2004) found females to have 48% lower calf venous compliance than males and
Meendering et al. (2005) reported a 26% greater compliance in the males than the females. The
magnitude of the reported gender differences is likely attributable to the way the compliance
differences were quantified and/or the fitness levels of the participants, which weren’t reported in the
previous studies. In pursuit of the mechanism responsible for differences in calf venous compliance
Venous Compliance in Trained Females
0.16
0.14
Average Female
Average Male
0.12
Compliance (ml/dl/mmHg)
between men and women,
Meendering et al. (2005)
measured
calf
venous
compliance during the early
follicular,
ovulatory,
and
midluteal phases of the
menstrual
cycle,
and
compared these findings to
men. Their data showed that
females had lower calf venous
compliance than males but
also suggested that calf
venous compliance does not
change with menstrual cycle
phase (4) and therefore
gender differences in venous
compliance are probably not
related to fluctuating hormone
levels.
45
Endurance Trained Female
0.1
Endurance Trained Male
0.08
0.06
0.04
0.02
0
0
10
20
30
Pressure (mmHg)
40
50
60
Figure 3.
Figure 3.
Compliance-Pressure slopes for average females,
average males, endurance trained females, and endurance trained
males.
Slope of Compliance
Recently, Lindenberger and
Lanne (2007) assessed sex
differences in venous compliance in the lower limb using three different levels of lower body negative
pressure (LBNP) as opposed to the cuff pressure application method utilized in the present
investigation and others (,5,7,14,18). They found that calf venous compliance was reduced in women
compared to men only at low
0
transmural pressures (11 & 22
mmHg) but disappeared at a higher
0.0005
pressure (44 mmHg). Further, they
found that capillary fluid filtration was
greater in the females than the males
0.001
at the lower distending pressures,
probably due to a higher capillary fluid
0.0015
coefficient in the women. The sex
differences in compliance were not
seen when the contribution of
0.002
capillary filtration was not accounted
for (18). The present investigation
0.0025
assessed compliance during pressure
reduction at a rate of 5 mmHg/5
Endurance Trained
Average Female
Average Male
Female
Endurance Trained Male
seconds (Figure 1) which should have
0.003
been fast enough to remove the
Figure 4. Slope of the compliance-pressure relationship. potential effects of differences in
Means + SD. ap<.05 vs average females; bp<.05 vs average capillary
fluid filtration
and
males
characterize volume changes over a
large pressure range (10-60 mmHg; 15). If capillary filtration differences between men and women
are driving the compliance differences that have been seen previously, then the method utilized in the
current investigation should consistently reveal no sex difference in compliance, but that has not been
the case. Whether this is due to the methodology or the fact that capillary filtration is not affecting
compliance assessment requires further investigation.
ab
ab
Venous Compliance in Trained Females
46
One possible explanation for the discrepancy in our current findings compared to previous research
showing that young females have lower venous compliance than males may be that our average fit
males and females had a higher body mass and BMI than that reported in previous studies (6,7,18).
The average females had a bodyfat percentage of 29.8 versus 17.7 in the average males. Oren et al.
(1996) assessed arterial and venous compliance using central blood volume indices and reported that
obesity increased central arterial compliance but had no effect on the capacitance of the venous
system (21). However, Stepniakowski and Egan (1995) reported reduced venous dispensability in
the forearm of obese individuals (22). Neither of these studies assessed venous compliance in the
lower limb or across a range of distending pressures. Obesity has been associated with an increased
resting
muscle
7
sympathetic
nerve
activity, but as Monahan
6
and
Ray
(2004)
demonstrated,
5
1.5528
sympathoexcitation
in
1.2364
females doesn’t appear
to
alter
venous
4
compliance. Therefore,
1.2374
0.8526
if females have less
3
compliant veins than
males as suggested
4.2988
4.221
previously (6,7,18), then
2
it’s possible that the
2.8824
2.8136
equivalent
compliance
1
found in the present
study may be due to the
0
higher body fat of the
Endurance Trained Female Endurance Trained Male
Average Male
Average Female
females.
The role
Capillary Filtration
Capacitance
obesity
plays
in
alterations of venous
Figure 5. Contribution of capacitance response (solid bars; bottom) and
compliance
deserves
capillary filtration response (shaded bars; top) to increases in calf
further investigation. To
volume with cuff pressure application of 60 mmHg for 8 minutes. Means
date,
mechanisms
+ SD. ap< 0.05 vs. average females; bp< 0.05 vs. average males; cp<0.05
associated with gender
vs. endurance trained male
differences
have
primarily focused on hormonal contribution (6), responses to baroreceptor unloading (7), and capillary
filtration differences (18). Gender differences in the structure of the vessel wall are yet unknown,
although estrogen receptors have been found in smooth muscle cells and may affect cellular
transcription of elastin and collagen (23,24). Future endeavors may want to match participants on
body fat levels as well as the fitness, age and gender of the participants when determining lower limb
venous compliance.
Calf Volume Increase (ml/dl)
abc
ab
ab
Several limitations should be considered when evaluating the results of this investigation. First, in
utilizing venous occlusion plethysmography to non-invasively assess venous compliance, the venous
collecting cuff pressure is used as a substitute for venous pressure; therefore this is really a measure
of whole limb compliance. Secondly, the participants included endurance athletes who participated in
sports involving the lower limbs; it is likely any adaptation to endurance exercise may be localized in
the trained limbs. Therefore, it is possible that different results may be observed if venous circulation
in other areas of the body is studied such as in the pelvic region where women tend to pool more
Venous Compliance in Trained Females
47
blood than men (7), or in athletes who train using a predominantly gravity independent environment
such as swimming. Lastly, only young healthy adults were investigated in the present study.
Therefore, our results cannot be generalized to other age groups or patients with other conditions.
CONCLUSIONS
In conclusion, endurance trained females have greater calf venous compliance than their more
sedentary peers. While previous studies have shown that females have lower calf venous
compliance than males (6,7), this investigation found that there was no difference between the sexes
in either the highly trained group or the groups of average fitness. More investigation into potential
sex differences is necessary to determine what is causing these discrepant findings.
Address for correspondence: Juliane P. Hernandez, Ph.D., Department of Kinesiology, 1075 S.
Normal, Southern Illinois University, Carbondale, IL 62915-4310. Phone (618)453-3124; FAX:
(618)453-3329; Email. juliane@siu.edu.
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Venous Compliance in Trained Females
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