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DOI: 10.1111/j.1471-0528.2006.01056.

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www.blackwellpublishing.com/bjog
General obstetrics

Uterine blood flow during supine rest and


exercise after 28 weeks of gestation
RM Jeffreys,a W Stepanchak,a B Lopez,a,b J Hardis,a JF Clapp IIIa,b,c
a Department of Obstetrics and Gynecology and the Schwartz Center for Metabolism and Nutrition, MetroHealth Medical Center, Cleveland,

OH, USA b Department of Reproductive Biology, Case Western Reserve University School of Medicine, Cleveland, OH, USA
c Department of Obstetrics and Gynecology, University of Vermont College of Medicine, Burlington, VT, USA

Correspondence: Dr JF Clapp III, Department of Obstetrics and Gynecology, MetroHealth Medical Center, 2500 MetroHealth Drive, Cleveland,
OH 44109, USA. Email jfclapp@metrohealth.org

Accepted 19 July 2006. Published OnlineEarly 15 September 2006.

Objective To test the null hypothesis that, after 28 weeks of Main outcome measures Blood pressure, heart rate, and uterine
gestation, uterine blood flow during supine rest and supine artery volume flow.
exercise is no different than uterine blood flow at left-lateral rest.
Results Data are presented as the mean SD. Maternal heart rate
Design In vivo experimental study in pregnant women. and blood pressure were unchanged at supine rest but increased
during supine exercise (heart rate increased from 76 9 to 98 12
Setting Department of Obstetrics, MetroHealth Medical Center,
beats per minute, mean arterial pressure increased from 81 6 to
Cleveland, OH, USA.
102 12 mmHg). Volume flow fell from 410 93 to 267 73 cc/
Population Fourteen, physically active, late-pregnant women who minute after 5 minutes of supine rest and then, during supine
continued supine exercise throughout gestation. exercise, increased to 355 125 cc/minute. Uterine artery luminal
diameter and blood flow correlated directly with tissue weights at
Methods Studies were carried out between 29 and 38 weeks of
birth (r2 values between 0.32 and 0.59).
gestation. Maternal blood pressure, maternal heart rate, and
ultrasound estimates of volume blood flow in the right ascending Conclusions In physically active women, uterine blood flow
branch of the uterine artery were obtained serially at rest in the decreases during both supine rest and supine exercise but the
left-lateral position, at rest in the supine position, during and decrease in the former is twice that seen in the latter.
immediately after 10 minutes of supine exercise, and again at rest
Keywords late pregnancy, supine exercise, supine rest, uterine
in the left-lateral position. Exercise sessions included alternating
blood flow
60- to 90-second periods of abdominal crunches and leg exercise at
moderate/high intensity (Borgs rating of perceived exertion 14 1).

Please cite this paper as: Jeffreys R, Stepanchak W, Lopez B, Hardis J, Clapp III J. Uterine blood flow during supine rest and exercise after 28 weeks of gestation.
BJOG 2006;113:12391247.

decreased venous return and cardiac output coupled with


Introduction
peripheral vasoconstriction and flow redistribution away
This study is part of a continuing comprehensive assessment from the splanchnic and uterine circulations. The early xenon
of the interaction between the physiological changes which clearance studies of Kauppila et al.2 demonstrated that inter-
occur during pregnancy and those associated with various villous space blood flow fell 34% when asymptomatic, late-
forms of exercise. It was designed to determine if the obstetric pregnant women changed from a 45 left-lateral tilt position
recommendation that healthy, physically active, late-pregnant to the supine position and the classic studies of Howard et al.3
women discontinue supine floor exercise is warranted.1 and Lees et al.4 documented that femoral venous pressure rose
The recommendation is based on the results of studies that while cardiac output and blood pressure fell when late-
have examined the effects of posture and exercise on maternal pregnant women changed from the position of left-lateral rest
haemodynamics in late pregnancy. The studies which have to supine rest. The studies by Clark et al.5 also demonstrated
examined posture indicate that uterine blood flow may fall that cardiac output fell when healthy, asymptomatic, preg-
dramatically in the supine position due to compression of nant women changed from a position of lateral to supine rest
the inferior vena cava by the pregnant uterus producing late in pregnancy and Ikeda et al.6 observed a 20% decrease in

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Jeffreys et al.

the mean flow velocity in the internal carotid artery with the
same positional change in healthy women in the third tri-
Methods
mester. General
Only one study has assessed the effects of supine exercise The protocol was approved by the MetroHealth Human
following a period of supine rest. That study was performed Experimentation Committee. All 14 subjects were healthy,
by Morris et al.7 and demonstrated that myometrial clearance non-substance-abusing, physically active women who had
times decreased by an average of 33% from those at supine continued regular supine floor exercise beyond the 28th week
rest during moderate intensity supine cycling. Several studies of gestation. In addition to regular floor exercise (two to six
have examined the effects of upright exercise on flow redis- times a week), all the women regularly (three to six times
tribution away from the splanchnic and uterine circulations a week) participated in other forms of exercise (30+ minutes
with mixed results. Ultrasound measurements of portal vein of aerobics, running, kick boxing, yoga, or weight training) at
blood flow indicate that treadmill exercise decreases splanch- moderate to high intensity (Borgs18 rating of perceived exer-
nic blood flow by more than 50% during mid and late human tion between 13 and 17). All were carrying singletons, had
pregnancy,8 while xenon clearance studies indicate that uter- experienced an uncomplicated antenatal course, and lived at
ine blood flow is unchanged following bicycle exercise.9 How- altitudes under 100 m. Fourteen initial studies were con-
ever, multiple studies in pregnant sheep reviewed elsewhere10 ducted between 28 and 34 weeks of gestation (31 2 weeks)
demonstrate dramatic decreases in uterine blood flow during and eight of the 14 women were able to return for a second
treadmill exercise. study between 35 and 38 weeks of gestation (36 1 weeks).
Nonetheless, we had multiple concerns about the use of The data from the 14 initial experiments were used to exam-
these findings to formulate recommendations for active, ine the responses to supine rest and supine exercise and the
healthy, pregnant women. First, our anecdotal experience eight sets of paired data were used to detect any potential
indicated that pregnancy outcomes were normal in women gestational age effect on the outcome variables.
who chose to continue supine exercise throughout their preg- In all women, dating was confirmed by an ultrasound at
nancies. Second, the magnitude of the changes in cardiac out- 2426 weeks of gestation and neonatal morphometrics and
put and splanchnic blood flow at supine rest in asymptomatic placental weight were obtained in a standardised fashion by
women was far less than those observed during quiet stand- an independent observer at the time of birth.19 Birthweights
ing5,8 or weight-bearing exercise.8 Third, the women who were corrected for gestational age, sex, and race using norma-
were studied by Morris et al.7 were presumably sedentary, tive data from our obstetric populace.19,20 Then, a corrected
and had been at bedrest for some time. These two factors total tissue weight was calculated as the sum of corrected
are known to decrease plasma volume and, therefore, should birthweight and placental weight.
alter venous return, preload, cardiac output, and regional
flow responses.5,11,12 Also, the technique used to estimate Experimental protocol
uterine blood flow measured the clearance rate of a tracer Each study was conducted in the MetroHealth Fetal Diagnos-
injected directly into the myometrium and probably did not tic Center between 1 and 3 pm, 90120 minutes after eating.
reflect changes in placental perfusion per se.9 Fourth, the only No attempt was made to control hydration prior to study.
study that directly assessed the effect of exercise on intervil- Upon arrival, a brief history documenting the subjects ante-
lous blood flow found no change and recent animal studies natal course, recent weight, and exercise habits was obtained.
document that the uterine vasoconstrictive response to exer- Then she was placed in the left-lateral decubitus position and
cise is halved in late pregnancy.9,13 an automated sphygmomanometer was placed on her left
Therefore, we designed this study to directly assess the arm. During the experiment that followed, multiple measure-
effect of supine rest and exercise on uterine blood flow in ments of each parameter were obtained under each of the four
healthy, fit women during late pregnancy. The null hypothesis experimental conditions (left-lateral decubitus rest, supine
tested was that uterine blood flow during supine rest and rest, supine exercise, and lateral recovery), and the average
supine exercise is no different than uterine blood flow at value obtained was used in the statistical calculations.
left-lateral rest after 28 weeks of gestation. After 5 minutes of rest in the left-lateral decubitus position,
A secondary interest was to determine if there is a relation- maternal blood pressure and heart rate were measured in
ship between the rate of uterine blood flow and fetoplacental triplicate at 2-minute intervals while duplicate estimates of
weight in the human. A direct linear relationship is present in volume flow in the ascending branch of the right uterine
multiple animal models but the issue has not been examined artery were obtained using a modification of the technique
in human pregnancy.1417 Therefore, the data were also used initially described and validated by Palmer et al.21 The mod-
to determine if there was a correlation between the basal or ifications included the use of colour flow Doppler for vessel
resting rate of uterine blood flow in the third trimester and identification and localisation of the measurement site as well
fetoplacental weight at the time of birth. as simultaneous measurement of flow velocity and vessel

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Uterine flow during supine rest and exercise

diameter. The fetal heart rate was then recorded before the employs a scale of 620. It has been shown to be a valid
subject was asked to shift to the supine position. No attempt estimate of relative exercise intensity in both the pregnant
was made to identify the site of placentation. and nonpregnant state and all the subjects were familiar with
After 3 minutes of rest in the supine position, measure- the technique and used it on a daily basis to assess their
ments of maternal heart rate and blood pressure were begun exercise intensity.18,22 A metronome was used to establish
and repeated at 2-minute intervals. After 5 minutes, duplicate and maintain cadence.
estimates of volume flow through the ascending branch of the Volume flow in the ascending branch of the right uterine
uterine artery were obtained at the same point in the vessel as artery was estimated by a single experienced ultrasonographer
those obtained at left-lateral rest. Then the fetal heart rate was who was blinded to both the studys hypothesis and each
briefly recorded. subjects exercise history. All measurements were obtained
The subject then began supine exercise. The duration and at rest because initial attempts at measurement during exer-
sequence of the exercise routine were standardised and were cise were unsuccessful.
designed to mimic that used in most health club floor exercise An Acuson/Siemens Sequoia machine (Acuson/Siemens,
sessions. The exercise session was 10 minutes in length and Malvern, PA) with a multi-frequency probe set at 4 or 5
the exercise sequence included 60- to 90-second intervals of MHz was used. Initially, the probe was placed 37 cm above
abdominal crunches (flexion of the head, neck, and upper the inguinal ligament, approximately one-third of the way
thorax on the trunk) alternating with 6090 seconds of either between the anterior superior iliac spine and the symphysis
leg lifts (flexion of extended legs on the trunk) or cycling pubis, and the vessel segment to be insonated was identified
motions (alternating thigh flexion and extension on the by its anatomic location (medial and inferior to the external
trunk) at a cadence of 60 moves per minute. Each subject iliac artery) and waveform shape (continuous high diastolic
was asked to exercise at her usual intensity. Maternal flow velocity) with colour flow Doppler. Then an easily rec-
blood pressure and heart rate measurements were begun at ognisable segment with a reproducible waveform (23 cm
3 minutes and repeated during each set of leg exercises and at medial to its crossing over the external iliac artery) was chosen
completion of the exercise. Duplicate volume flow estimates and pulsed wave Doppler was used to measure the time-averaged
in the ascending branch of the right uterine artery were velocity of flow over three cycles (calculated electronically
obtained at the same point in the vessel during a 10- to 20- from pixel densities) with simultaneous measurement of
second pause in the exercise at 5 minutes and again within the vessel luminal diameter at the point of insonation. No
1020 seconds of exercise cessation at 10 minutes. Then a brief attempt was made to correct the diameter measurement for
measurement of fetal heart rate was obtained, the subject changes in the cardiac cycle. Volume flow through the vessel
returned to the left-lateral rest position, and a final set of was calculated as the product of the luminal cross-sectional
measurements was obtained after 2 minutes of recovery in area [(diameter/2)2 3.1416] and the time-averaged flow
that position. velocity. The coefficient of variation for the paired measure-
Throughout the study, care was taken to ensure that the ments of time-averaged velocity, diameter, and estimated
table was flat and to standardise the positions in which meas- volume flow were 16, 8, and 11%, respectively. Uterine
urements were made. When in the left-lateral position, the vascular resistance was calculated from the data in peripheral
subject lay with her back vertical, knees slightly flexed, left resistance units (mmHg/ml/second).
arm extended, and right arm resting on her right side. When
at supine rest she lay flat with one or two folded towels under Data management
her head, left arm extended laterally, and right arm at her side. The level of significance was set at a P value <0.05. The sample
During the abdominal crunches knees were slightly flexed and size necessary to detect a change in volume flow of 10% at that
during leg exercise the trunk was flat and the left arm level with a power of 0.80 was calculated to be 8 using the
extended laterally. variance data obtained in our earlier studies of portal vein
blood flow.8 The outcome parameters of interest were mater-
Measurement techniques nal blood pressure and heart rate, fetal heart rate, time-
Maternal blood pressure and heart rate were estimated over averaged uterine artery flow velocity, uterine artery luminal
a 30- to 45-second interval with an Omron 711 automatic diameter, calculated volume flow and vascular resistance, and
portable monitor (Omron Matsusaka Co., Bannockburn, IL) the relationships among uterine artery luminal diameter, the
whose accuracy was periodically checked against a mercury rate of uterine blood flow, and tissue weight at birth.
manometer and a portable heart rate monitor. In the left- The ShapiroWilk normality test indicated that the param-
lateral position the device was zeroed at the mid-clavicular eters of interest were normally distributed in all four posi-
line and, in the supine position, at the mid-axillary line. Fetal tions. Significant changes in the outcome parameters of
heart rate was obtained by ultrasound. Exercise intensity was interest with changes in position and exercise were sought
assessed using Borgs18 rating of perceived exertion. This with the data from the initial 14 experiments using repeated

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Jeffreys et al.

measures analysis of variance followed by Tukeys test. Linear Mean birthweight was 3658 417 g (range 28104706 g) and
regression was used to examine the relationships among uter- mean corrected birthweight was similar (3719 346 g).
ine artery luminal diameter, volume flow in the ascending Ponderal indices ranged between 2.30 and 3.12 (2.71
branch of the right uterine artery, and corrected birthweight, 0.26) and placental weights ranged between 365 and 550 g.
placental weight, and total corrected weight (corrected birth- Total corrected weight (corrected birthweight + placental
weight + placental weight) in the 14 initial experiments and weight) ranged between 3509 and 5106 g (4188 385 g).
separately in the eight repeat studies. Linear regression was Neonatal courses were unremarkable.
also used to assess relationships among other variables mea-
sured and the between-experiment variability in the flow Changes in maternal heart rate and
response. The paired t test was used to detect changes in the blood pressure
parameters of interest with advancing gestation. The heart rate and blood pressure responses to positional
All data obtained in a single position were averaged and the change and supine exercise in the initial 14 experiments are
mean values were used in the statistical calculations. Statistix presented in Table 1. They were qualitatively and direction-
8 software (Statistix, Tallahassee, FL) was used for data anal- ally similar in all subjects at both gestational ages and, in the
ysis. Blood pressure, heart rates, flow velocities, and luminal eight women who were studied twice, there were no changes
diameters are reported as the mean SD while volume flow in magnitude with advancing gestation.
and vascular resistance estimates are reported both numeri- Maternal heart rate was unchanged from that recorded in
cally and as percent change from those at either left-lateral the left-lateral position after 35 minutes of supine rest but
rest or supine rest. was significantly elevated (P < 0.0001) during and immedi-
ately after the last 7 minutes of supine exercise. The heart rate
obtained immediately after exercise was similar to the last
Results
measurement obtained during exercise. After 2 minutes of
General recovery at left-lateral rest, heart rate fell to a level not signif-
Mean maternal age was 34 3 years (range 2938 years), icantly different from the initial value obtained after
parity ranged from zero to four, and historical nonpregnant 5 minutes of left-lateral rest.
mean weight and height were 59.1 4.2 kg and 169 5 cm, Maternal blood pressure followed a similar pattern with no
respectively. At the time of study, the body mass index ranged significant change during supine rest but it increased signif-
from 18.4 to 29.6 (24.5 2.8). The mean gestational age for icantly (P < 0.0001) during and immediately after supine
the 14 initial studies was 31 2 and 36 1 weeks for the eight exercise. The average blood pressure obtained during exercise
repeat studies. was virtually identical to that recorded immediately after
Fetal heart rate at left-lateral rest was unchanged after exercise (1 2 mmHg). After 2 minutes of recovery, blood
5 minutes of supine rest (136 10 versus 137 11 beats per pressure had returned to initial levels.
minute [b.p.m.]). However, it increased significantly (P <
0.02) after 10 minutes of supine exercise (144 15 b.p.m.) Changes in uterine artery luminal diameter
and then returned to the initial level by the third minute of and flow velocity
recovery (137 8 b.p.m.). Exercise intensity using Borgs sub- The changes in uterine artery luminal diameter and flow
jective rating of perceived exertion ranged between 13 and 17 velocity in response to position change and supine exercise
(moderate to very hard) with a mean rating of 15 1(hard). were qualitatively similar in all 14 initial experiments. They
Labour onset occurred at term in all women [range = 268 are detailed in Table 2. There were no significant changes
289 days, (277 6 days)] and was uncomplicated in 13 of 14. with advancing gestation in the eight women who were stud-
The remaining labour was complicated by shoulder dystocia. ied twice.

Table 1. Maternal heart rate and blood pressure responses to positional change and supine exercise in the initial 14 studies

Parameter Left-lateral rest Supine rest Supine exercise Lateral recovery

Heart rate (b.p.m.) 76  9 78  9 98  12* 78  9


Systolic pressure (mmHg) 112  11 110  12 133  13* 111  15
Diastolic pressure (mmHg) 66  6 67  10 86  12* 67  10
Mean pressure (mmHg) 81  6 81  10 102  12* 82  10

Data are presented as the mean  SD.


*P , 0.001 versus all resting positions.

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Uterine flow during supine rest and exercise

Table 2. Changes in uterine artery luminal diameter and flow velocity with positional change and supine exercise in the initial 14 studies

Parameter Left-lateral rest Supine rest Supine exercise Lateral recovery

Luminal diameter (mm) 4.9  0.8 4.2  0.8* 4.3  0.8* 4.8  0.9
Flow velocity (cm/sec) 38  13 32  11* 43  14 37  13

Data are presented as the mean  SD.


*P , 0.001 from left-lateral rest.

After 5 minutes in the left-lateral rest position, luminal ing gestation while the systolic/diastolic ratio was unchanged
diameter of the ascending branch of the uterine artery was (2.2 0.4 and 2.1 0.4, respectively).
4.9 0.8 mm. After 5 minutes of supine rest, the diameter After 5 minutes of rest in the left-lateral position, mean
consistently decreased (P < 0.0001) to 4.2 0.7 mm and did volume flow for the initial 14 studies was 410 93 cc/minute.
not change further after 5 and 10 minutes of supine exercise Five minutes after changing to the supine rest position, vol-
(4.3 0.8 mm). After returning to left-lateral rest, luminal ume flow decreased in all women (34 11%) to a mean value
diameter increased (P < 0.05) to a level not significantly dif- of 267 73 cc/minute (P < 0.0001). During supine exercise
ferent from the baseline value. volume flow rose in all women. The mean value (355 125
After 5 minutes of rest in the left-lateral rest position time- cc/minute) was significantly greater than that observed at
averaged flow velocity in the vessel was 38 13 cm/second. supine rest (P < 0.003) but was not significantly different
After 5 minutes of supine rest, velocity fell consistently (P < from that observed during either baseline or recovery left-
0.009) to a mean value of 32 11 cm/second. However, after lateral rest.
5 and 10 minutes of supine exercise, it rose significantly (P < The variability in the magnitude of the flow increase during
0.0006) to a level similar to that obtained initially at left- supine exercise (88 87 cc/minute or 33 32%) was also of
lateral rest (43 14 cm/second, P < 0.15). After 2 minutes interest. On five occasions it actually rose above the level
of left-lateral recovery, it was 37 12 cm/second, a value not observed at left-lateral rest and on three others the increase
significantly different from that observed either at baseline was less than 10% above that obtained at supine rest. These
left-lateral rest or during supine exercise. differences in response did not appear to be technical artefact
as the within-subject coefficient of variation between the 5-
and 10-minute estimates was similar to that for the estimate
Estimated volume flow, vascular resistance, itself (14 versus 11%) with an average difference between
and the systolic/diastolic flow/velocity ratio the two estimates of 3 31 cc/minute. Therefore, an attempt
in the uterine artery was made to identify potential explanatory variables. The
The responses in the initial 14 experiments are presented in magnitude of the flow increase did not correlate significantly
Table 3. They were directionally similar in all subjects and the with subjective exercise intensity (P = 0.54), initial flow rate
response pattern to changes in position and exercise was not (P = 0.92), flow rate at supine rest (P = 0.94), or maternal
altered with advancing gestation. However, in the eight pressor response (P = 0.16). However, significant correlations
women studied twice, volume flow at left-lateral decubitus were present between the magnitude of the flow response and
rest rose significantly (394 57 to 504 103 cc/minute, birthweight, corrected birthweight, and total corrected weight
P < 0.0001) and calculated vascular resistance fell (12.1 (r2 values between 0.44 and 0.49, P values between 0.01 and
1.9 to 10.1 2.4 mmHg/ml/second, P < 0.0001) with advanc- 0.005).

Table 3. Changes in uterine blood flow and vascular resistance with positional change and supine exercise in the initial 14 studies

Parameter Left-lateral rest Supine rest Supine exercise Lateral recovery

Blood flow (cc/minute) 410  93 267  73* 355  125 409  170
Percent change from left-lateral rest 0 234  11* 216  23 21  30
Vascular resistance (mmHg/ml/sec) 12.4  3.0 19.5  6* 18.6  6.5* 13.9  4.8
Systolic/diastolic ratio 2.0  0.4 2.0  0.6 1.9  0.2 1.9  0.3

Data presented as the mean  SD.


*P , 0.002 from left-lateral rest.

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Jeffreys et al.

After 5 minutes of rest in the left-lateral position calculated


Discussion
vascular resistance was 12.4 3.0 mmHg/ml/second. It rose in
all the 14 initial studies by an average of 56% to 19.5 6.0 The observation that uterine blood flow in the ascending
mmHg/ml/second after 5 minutes of supine rest (P < 0.0001) branch of the uterine artery decreased 34% at supine rest is
and then fell insignificantly (P = 0.40) after 5 and 10 minutes not a new finding and is identical in magnitude to that
of supine exercise (18.6 6.5 mmHg/ml/second). After reported earlier by Kauppila et al.2 using a clearance tech-
2 minutes of left-lateral recovery, it fell significantly (P < nique. However, the ultrasonic technique used in the current
0.01) to a level that was not significantly different (P = study, also allowed us to determine that two-thirds of the
0.29) from the baseline value. reduction in flow was the result of a decrease in the vessels
After 5 minutes of rest in the left-lateral position the sys- luminal cross-sectional area and only one-third the result of
tolic/diastolic velocity waveform ratio was 2.0 0.4. As shown a fall in velocity. This uterine vasoconstrictive response to
in Table 3, it did not change significantly after 5 minutes of a decrease in venous return and cardiac output35 is a new
supine rest, 10 minutes of supine exercise, or 2 minutes of finding and the fact that the luminal diameter did not
recovery in the left-lateral position. Thus, it did not reflect decrease further during supine exercise suggests that the ini-
either changes in volume flow or calculated vascular resis- tial response was near maximal for this bed in late pregnancy.
tance in the uterine circulation. Earlier observations made in women with the supine hypo-
tensive syndrome demonstrated that uterine flow rate fell at
The relationships among uterine artery luminal supine rest in symptomatic women,3,23 and it was assumed
diameter, volume flow, and tissue weight at term that the fall was due to the decrease in arterial pressure which
As anticipated, the rate of uterine blood flow in the 14 initial decreased flow velocity. Likewise, the studies of Kauppila
studies correlated directly with the luminal diameter of the et al.2 and Kinesella et al.24 in asymptomatic women sug-
uterine artery both at left-lateral rest (r2 = 0.37) and during gested that the fall in intervillous and femoral blood flow
supine exercise (r2 = 0.50). Uterine blood flow also correlated in the supine position was due to aortocaval compression
directly with corrected birthweight, placental weight, and total producing a decrease in perfusion pressure. The possibility
corrected tissue weight (r2 values between 0.32 and 0.37). of vasoconstriction was not considered because earlier work
Similar but stronger relationships were present among luminal had demonstrated that, in late human pregnancy, general
diameter (both at left-lateral rest and during supine exercise) vascular reactivity is blunted, sympathetic nerve endings in
and corrected birthweight, placental weight, and total cor- the uterine arteries are markedly reduced, and uterine blood
rected tissue weight (r2 values between 0.44 and 0.59, P values flow is pressure passive.13,2527 Thus, the finding of vasocon-
all <0.01). The strongest of these is shown in Figure 1. Signif- striction in a large uterine vessel during supine rest was
icant correlations were also present among the uterine artery unanticipated but consistent with our earlier findings of
luminal diameter, flow rate, and corrected birthweight, placen- vasoconstriction in the splanchnic circulation at standing rest
tal weight, and total corrected tissue weight (r2 values between in late pregnancy.8
0.34 and 0.58, P values all <0.05) in the eight studies conducted The observation that vasoconstriction occurs during
between the 35th and 38th week. supine rest in normal pregnant women suggests that vaso-
constriction in the uterine circulation during mid and late
pregnancy probably is a normal response to a variety of hae-
modynamic stimuli that are a part of everyday life. If this is
indeed the case, then the rate of uterine blood flow probably
varies widely throughout any 24-hour period, suggesting that
there is a large margin of reserve within the uteroplacental
circulation. Further experiments will be necessary to provide
objective evidence that this supposition is correct but it is
probable that changes in uterine vascular resistance will fol-
low those in the general systemic circulation in response to
changes in cardiac output.5
The finding that uterine blood flow during supine exercise
increases above the level present at supine rest in asymptom-
atic, physically active women is another new finding which
Figure 1. The relationship between the luminal diameter of the uterine
does not support the specific portion of the American College
artery during supine exercise and corrected tissue weight at term in the
initial 14 studies. R2 = 0.5889. The relationship is described by the
of Obstetricians and Gynaecologists guidelines that prohibits
following formula: tissue weight = 2600 + 37.4 the uterine artery supine exercise in all women.1 Indeed, the increase in uterine
luminal diameter in millimetres. flow rate appears to be proportional to the tissue mass that is

1244 RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology


Uterine flow during supine rest and exercise

being perfused which is clearly fetoprotective. As acute exer- tionship between flow rate and tissue weight at term reflects
cise-induced decreases in uterine blood flow of greater mag- the effect of the rate of tissue growth within the uterus on the
nitude are clearly well tolerated by the fetus in both animals luminal diameter and reactivity of the uterine artery.
and man,2,8,10,22 this level of blood flow should not be a reason The strong relationship amongst uterine artery luminal
for clinical concern in healthy, asymptomatic women who diameter, the rate of uterine blood flow during the third tri-
choose to continue supine exercise in late pregnancy. On mester, and tissue weights at term is a third new finding and is
the other hand, the same is not true for supine rest, especially similar to that seen in ovine pregnancy.1416 This may explain
if protracted, or in either symptomatic or anaesthetised the marked betweensubject variability in the basal rate of
women.3,4,23,24,28 uterine blood flow seen in the current study. It explains the
The increase in uterine flow during supine exercise con- between-subject variability in uterine blood flow and suggests
flicts with the earlier work of Morris et al.7 The reason for the that the measurement of either uterine artery diameter or
conflict is unclear but we speculate that it is the result of two uterine blood flow under defined conditions may have clinical
factors. First, as noted earlier, there were marked differences value as screening tools for both fetal growth restriction and
between both the subject characteristics and the experimental overgrowth. It is well known that diseases which chronically
protocol. Second, different methodologies were used to reduce placental perfusion or placental size are associated
assess flow. In the current study the measurement of volume with growth restriction, whereas overgrowth is associated
flow was direct and had a relatively low coefficient of vari- with large placentas and, in the current study, high rates of
ation while the earlier study estimated myometrial clearance uterine blood flow.15,29 Clearly, more work needs to be done
rather than uterine flow and required between 6 and 12 both to confirm this supposition and to develop normative
minutes. The potential error inherent in the latter is rein- standards.
forced by the findings of Rauramo and Forss9 who, like The uterine blood flow values initially obtained at left-
Kauppila et al.,2 used an intravenous marker which produced lateral rest in the current study are higher than those reported
both a placental and myometrial wash-out curve. They by both Palmer et al.21 and Thaler et al.30 In all probability, the
reported that upright cycle ergometry had no effect on pla- differences are due to a combination of factors including
cental blood flow. differences in positioning and time, the equipment used,
The mechanisms underlying the decrease in uterine blood the analytic algorithm used, and the subject populace. Palmer
flow at supine rest followed by an increase with the onset of et al.21 collected data over 2 hours in the supine position with
exercise appears to be related to concomitant changes in a hip wedge in place which may have been inadequate to
venous return, cardiac output, blood pressure, and vascular maintain uterine volume flow at the same level as that present
resistance in multiple vascular beds.210 The change in posi- during left-lateral rest over that time interval.24,28 Crawford
tion to supine rest was associated with concomitant et al.28 noted that cardiovascular responses of both mother
decreases in venous return and cardiac output which initi- and fetus deteriorated over time despite the use of a hip wedge
ated maximal vasoconstriction in the uterine vascular bed and Kinsella et al.24 report that lateral tilt using a Crawford
which was maintained during supine exercise. The increase wedge did not alter the cardiovascular effects seen with aor-
in flow rate during supine exercise was simply a function of tocaval compression at supine rest and the same should be
the exercise-induced increase in venous return, cardiac out- true for intervillous space blood flow.2 Thaler et al.30 obtained
put, and perfusion pressure that increased flow velocity and their measurements transvaginally in a shorter time period
volume flow through the vessel. It is of clinical interest that but their subjects were in the supine position and should also
none of the changes in flow or resistance were reflected by have had aortocaval compression.
changes in the systolic/diastolic velocity flow profile in the Our supine measurements were comparable with those
uterine artery. reported at a similar gestational age by both Palmer et al.21
The differences seen in magnitude of the flow increase and Thaler et al.30 (267 versus 275 cc/minute), and the mag-
during supine exercise were not related to the exercise regi- nitude of the decrease in flow when subjects changed from
men. Most aspects of the exercise regimen were standardised a left-lateral rest to supine rest observed in the current study
and the two that were not (exercise intensity and pressor (34%) was identical to the decrease in intervillous space clear-
response) were unrelated to the magnitude of the flow ance observed by Kauppila et al.2 (34%). Both suggest that the
response. However, significant direct correlations were pres- differences between our values and theirs were primarily due
ent between the magnitude of the flow response and both to changes with position and time.
vessel diameter and term tissue weights. This is surprising The equipment and software used by Palmer et al.21 were
and appears to reflect direct relationships among uterine specifically designed to estimate uterine volume flow and
artery vessel diameter (both at left-lateral rest and during were clearly more reproducible than ours. The fact that the
supine exercise), volume flow, and tissue weights at term. vessel diameters were 2025% smaller in both studies prob-
While this requires confirmation, it suggests that the rela- ably reflects, in part, a consistent overestimation when the

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology 1245


Jeffreys et al.

measurement is made using colour flow Doppler but some of 5 Clark SL, Cotton DB, Pivarnik JM, Lee W, Hankins GD, Benedetti TJ,
the difference may have been due to vasoconstriction in the et al. Position change and central hemodynamic profile during normal
third-trimester pregnancy and postpartum. Am J Obstet Gynecol
artery as our luminal diameters decreased by an average of 0.7 1991;164:8837.
mm at supine rest.21,30 The consistently higher flow velocities 6 Ikeda T, Ohbuchi H, Ikenoue T, Mori N. Maternal cerebral hemodynamics
reported by Palmer et al.21 reflect their decision to analyse in the supine hypotensive syndrome. Obstet Gynecol 1992;79:2731.
only the largest waveform series obtained over the period of 7 Morris N, Osborn SB, Wright HP, Hart A. Effective uterine blood flow
during exercise in normal and pre-eclamptic pregnancies. Lancet
study. In the current study, rapid, brief, three to six beat series
1956;2:4814.
were obtained in duplicate without specific selection after 8 Clapp JF, Stepanchak W, Tomaselli J, Kortan M, Fanselow S. Portal vein
a short, prescribed time interval. blood floweffects of pregnancy, gravity and exercise. Am J Obstet
Finally, the subjects of Palmer et al.21 were studied at an Gynecol 2000;183:16772.
altitude of 1600 m while ours were studied at sea level. This 9 Rauramo I, Forss M. Effect of exercise on maternal hemodynamics and
placental blood flow in healthy women. Acta Obstet Gynecol Scand
may have decreased both their blood volume and uterine
1988;67:215.
blood flow as both are reduced at high altitude.31 10 Lotgering FK, Gilbert RD, Longo LD. Exercise in pregnancy in the exper-
The current study has several limitations. First, the dura- imental animal. In: Mittlemark RA, Wiswell RA, Drinkwater BL, editors.
tion and intensity of the supine exercise was designed to Exercise in Pregnancy. Baltimore, MD: Williams and Wilkins; 1991.
mimic the routines commonly used in local health clubs p. 15774.
and it is entirely possible that a longer exercise session at 11 Pivarnik JM, Mauer MB, Ayres NA, Kirshon B, Dildy GA, Cotton DB.
Effect of chronic exercise on blood volume expansion and hematologic
a lower intensity could produce a different result. Second, indices during pregnancy. Obstet Gynecol 1994;83:2659.
we were unable to obtain measurements during the exercise 12 Saltin B, Blomqvist B, Mitchell JH, Johnson RL, Wildenthal K, Chapman
due to motion artefact and the values obtained when the CB. Response to exercise after bed rest and training. Circulation
exercise was stopped may have been slightly higher than those 1968;38(5 Suppl):VII178.
13 OHagan JP, Alberts JA. Uterine artery blood flow and renal sympa-
present during the exercise.10 Third, the coefficients of varia-
thetic nerve activity during exercise in rabbit pregnancy. Am J Physiol
tion for the measurement of vessel diameters and flow veloc- Regul Intergr Comp Physiol 2003;285:R113544.
ity in the current study were large. 14 Clapp JF, McLaughlin MK, Larrow RW, Farnham J, Mann LI. The uterine
In summary, these data do not support the original hemodynamic response to repetitive unilateral vascular embolization in
hypothesis. Uterine blood flow falls at supine rest primarily the pregnant ewe. Am J Obstet Gynecol 1982;144:30918.
15 Lang U, Baker RS, Braems G, Zygmunt M, Kunzel W, Clark KE. Uterine
because of uterine vasoconstriction in response to a decrease
blood flowa determinant of fetal growth. Eur J Obstet Gynecol
in both venous return and cardiac output. With the onset of Reprod Biol 2003;110:S5561.
supine exercise venous return, cardiac output, and blood 16 Lang U, Baker RS, Khoury J, Clark KE. Effect of chronic reduction in
pressure rise which increases uterine blood flow to a level uterine blood flow on fetal and placental growth in the sheep. Am J
significantly above that observed at supine rest in healthy, Physiol Regul Integr Comp Physiol 2000;279:R539.
17 Clavero-Nunez JA, Negueruela J, Ortiz L, De los Heros AJ, Modrego PS.
fit, late-pregnant women. The luminal diameter of the uterine
Blood flow in the intervillous space and fetal blood flow. I. Normal
artery, the basal rate of uterine blood flow, and the magnitude values in human pregnancies at term. Am J Obstet Gynecol
of its increase during supine exercise correlate with the tissue 1973;116:3406.
weights obtained at the time of delivery. 18 Borg GAV. Borgs Perceived Exertion and Pain Scales. Champaign, IL:
Human Kinetics, 1998.
19 Clapp JF, Kim H, Burciu B, Schmidt S, Petry K, Lopez B. Continuing
regular exercise during pregnancy: effect of exercise volume on feto-
Acknowledgements placental growth. Am J Obstet Gynecol 2002;189:1427.
20 Amini SB, Catalano PM, Hirsh V, Mann LI. An analysis of birth weight by
This study was supported by National Institutes of Health
gestational age using a computerized perinatal data base, 1975-1992.
grants HD21268, RR00080, and RR00109 and by Metro- Obstet Gynecol 1994;83:34252.
Health Medical Center. j 21 Palmer SK, Zamudio S, Coffin C, Parker S, Stamm E, Moore L.
Quantitative estimation of uterine artery blood flow and pelvic
blood flow redistribution in pregnancy. Obstet Gynecol 1992;80:
10006.
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