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TABLE OF CONTENTS
Introduction
Basis of Doppler ultrasound
Methods of analysis
Velocity waveform analysis
Uterine blood flow
Ovarian blood flow
Uterine blood flow in the first
16 weeks of normal pregnancy
Uterine blood flow in abnormal pregnancy
New areas of investigation
Conclusions
References
should be sent to: Fertility Institute of New Orleans, 6020 Bullard Avenue, New Orleans, LA 70128, USA. Telephone: (504) 2468971;
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Table I. Waveform classification
Original
classificationa
Revised
classificationb
Description
Present
classification
Type C
Type C
Type C
Type B
Type D-I
Type B
Type A
Type D-II
Type A
None
Type D-III
Type D
Type 0
Type D-IV
Type 0
None
Type N
Type N
aReprinted
bFrom
Methods of analysis
Doppler blood flow may be analysed in three ways by: (i)
waveform, (ii) resistance indices and (iii) flow volume or
velocity. There are situations in which each of these
methods of analysis is best and should be used, and
situations in which each is unreliable. Flow volume
analysis is the closest to true blood flow, but the most
difficult to perform, because it is dependent on the angle of
insonation, accurate measurement of vessel diameter, the
tortuosity of the vessel and the analytical power of the
instrumentation. Flow volume analysis can only be used
for larger vessels, such as the ascending uterine arteries, but
may sometimes be used for ovarian arteries and umbilical
vessels. Resistance indices measure downstream impedance to blood flow and are independent of the angle of
insonation, but are only indirect estimates of flow volume.
They are most useful for estimating blood flow in vessels
distal to the point of examination. Despite claims to the
contrary, resistance indices may be highly inaccurate when
blood flow in the vessel being measured is not continuous
throughout the cardiac cycle. Waveform analysis provides
the most accurate estimate of blood flow in conditions
Figure 1. Waveform type C. Uterine flow velocity waveform showing high systolic flow and diastolic wave extending to the next cardiac cycle. This indicates good uterine perfusion. Reprinted with
permission from Goswamy and Steptoe (1988).
Figure 2. Waveform type A. Uterine flow velocity waveform showing high systolic flow and absence of early diastolic flow. This indicates poor uterine perfusion. Reprinted with permission from Goswamy and Steptoe (1988).
471
Figure 3. Waveform type B. Uterine flow velocity waveform showing diastolic wave continuous with systole, but not extending to the
next cardiac cycle. This indicates good uterine perfusion. Reprinted
with permission from Goswamy and Steptoe (1988).
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R.P.Dickey
473
Other ratios
RI = (S D)/S
where S is the peak systolic velocity and D is the minimum
or end diastolic velocity. The RI is suitable for low
resistance vascular beds with continuous flow throughout
diastole. If the end diastole value (D) goes to zero, the ratio
converges to 1.
Pulsatility index (PI)
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Pulsatility index
RI
S/D ratio
Systolic/diastolic ratio
Vmax
MDV
PPI
PSV
MPSV
TAMV
TAMX
TAPV
475
The relationship of uterine artery waveforms to a modification of RI and S/D ratio was initially reported by Goswamy
and Steptoe (1988). More recently, the relationship of
ascending uterine artery and spiral artery waveforms to
uterine artery flow volume, PI and RI was investigated by
Dickey et al. (1994) (Table IV). Uterine artery flow volume
was significantly lower and PI was significantly higher when
waveforms were not continuous. Recumbent flow volume in
single (right or left) uterine arteries averaged 40.8 ml/min
when waveforms were continuous, compared to 27.0 ml/min
when only end diastole flow was absent (type B, D-I) and to
19.722.0 ml/min when flow was absent in early diastolic
flow (A and D, D-II and D-III). Uterine artery PI was
significantly higher for all non-continuous waveforms,
compared to continuous waveforms, and did not distinguish
waveforms of less clinical significance with absent end
diastolic flow only (type B, D-I) from waveforms of greater
clinical significance (A and D, D-II and D-III). Tekay et al.
(1996b) also reported on the relationship between waveform
type and PI.
Table III. Interobserver variability, showing the mean difference between observers 1 and 2, the correlation coefficient (r), standard error (SE) and standard deviation (SD). Reprinted with permission from Dickey et al. (1994)
Measurement
Mean difference
between 1 & 2
SE of mean
difference
SD of mean
difference
diameter (cm)
20
0.056
0.94
0.067
0.300
20
1.070
0.90
2.180
0.470
20
4.500
0.88
2.398
10.721
pulsatility index
20
0.067
0.95
0.066
0.296
resistance index
20
0.004
0.97
0.006
0.027
pulsatility index
10
0.208
0.87
0.061
0.193
resistance index
10
0.052
0.85
0.009
0.028
Uterine artery
Spiral artery
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Table IV. Relationship of ascending uterine artery blood flow volume per minute (UA-VOL, ml/min), pulsatility index (PI) and
resistance index (RI) to uterine artery waveforms and spiral artery waveforms while subjects were recumbent and while they
were standing. Values in each column for UA-VOL, UA-PI and UA-RI are mean and SE respectively. Reprinted with permission
from Dickey et al. (1994)
Waveform
Recumbent
classification*
Standing
UA-VOL
UA-PI
UA-RI
n
98
UA-VOL
UA-PI
UA-RI
0.87, 0.01
40.8, 2.3
2.47, 0.05
0.86, 0.01
D-I
(B)
27.0, 4.8a
3.47, 0.17b
D-II
(A)
19.7, 3.3b
3.59, 0.13b
D-III
(D)
17
22.0, 1.6b
3.36, 0.09b
D-IV
115
(0)
37.9, 2.6
2.47, 0.05
31
19.4, 1.9b
3.59, 0.13b
17
15.2, 2.8b
4.45, 0.41b
0.05b
3.0,
0.90b
9.95,
59
74.4, 5.8
2.63, 0.08
0.88, 0.01
59
65.4, 6.1
2.67, 0.15
0.87, 0.01
D-I
(B)
14
72.8, 11.6
2.90, 0.11
0.92, 0.02
80.4, 13.9
2.77, 0.18
0.93, 0.02
D-II
(A)
45.0,
3.31,
0.92,
D-III
(D)
46.0,
2.79,
0.88,
22.3, 3.0b
4.30, 64.0
1.00, 0.015
D-IV
(0)
D-V
(N)
40.0, 15.8
4.24,
1.18c
0.94, 0.04
Significance
Significance
0.49
0.46
0.46
0.28
P < 0.001
P < 0.001
P = 0.010
0.21
P = 0.042
0.08
P < 0.001
P < 0.001
NS
0.09
NS
0.66
0.24
P = 0.019
0.31
P = 0.005
0.26
P = 0.013
0.30
P = 0.006
0.24
P = 0.017
0.54
P < 0.001
0.33
P = 0.002
0.54
P < 0.001
477
Figure 6. Uterine artery waveform type, S/D (systolic/diastolic) ratio and resistance index (RI) in a multiparous subject during the
menstrual cycle. Reprinted with permission from Goswamy and
Steptoe (1988). For abbreviations, see Table I.
Figure 7. Uterine artery waveform type, S/D (systolic/diastolic) ratio and resistance index (RI) in a nulliparous subject during the
menstrual cycle. Reprinted with permission from Goswamy and
Steptoe (1988). For abbreviations, see Table I.
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R.P.Dickey
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
MDV
PI
RI
S/D
ratio
x
x
x
x
A = abdominal ultrasound; A/V = abdominal and vaginal ultrasound; C = circadian rhythm also studied; E = relationship to
oestrogen, progesterone and ovulation induction studied; IA = common, external and internal iliac arteries also measured; O =
ovarian blood flow also measured; S = spiral arteries also measured; STD = standing blood flow also measured. See Table II for
other abbreviations.
479
Table VII. Studies of uterine blood flow in in-vitro fertilization and infertility
Investigation and
when measured
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
MDV
PI
RI
S/D
ratio
(1988) (A) IV
Sterzik et al. (1989) (O) II
x
x
x
x
x
x
A = abdominal ultrasound; O = ovarian blood flow also measured; INF = infertility. I = measured on or before day of human
chorionic gonadotrophin administration; II = measured on day of oocyte retrieval; III = measured on day of embryo transfer; IV =
measured in mid-luteal phase. See Table II for other abbreviations.
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15% when the PI was 3.0 and to 10% when the PI was 3.5.
The pregnancy rate was 39% when the RI was <0.91,
compared to 13% when the RI was 0.92. The best cut-off
values were 3.3 for PI and 0.95 for RI. Absent diastolic
velocity was noted in only six patients, one of whom
conceived but aborted. Tekay et al. (1996b) measured flow
velocity waveform type, PI, MPSV and MDV with a 6 MHz
vaginal transducer on the day of embryo transfer in 25
patients during a GnRHHMG cycle, and in 32 patients
having frozen embryo transfer in spontaneous cycles. There
were no conceptions when both uterine arteries had flow
velocity waveforms with absent end diastolic flow (type B
and D or D-II and D-III). The mean PI was significantly
lower, and the mean MDV was significantly higher, but
mean MPSV was not different in GnRH-HMG cycles,
compared to spontaneous cycles. There were no differences
in mean PI, MPSV, or MDV between conception and
non-conception cycles among patients with continuous
diastolic flow. However, individual PI values were always
<4.0 in conception cycles.
Bassil et al. (1995) measured mean (right and left) uterine
artery RI with a 6.5 MHz vaginal transducer from the
beginning of HMG administration to the day of embryo
transfer in 152 patients (196 cycles) after GnRH. Only 102
cycles in which three good quality embryos were
transferred and in which endometrial thickness was 9 mm
were analysed. A significant increase in RI was seen during
7 days of stimulation, which stabilized for 3 days before
decreasing markedly from day 9 until day 13, when HCG
was given. After HCG administration, the RI increased
significantly until the day of oocyte retrieval, then
decreased slightly until embryo transfer. In cycles which
resulted in pregnancy, RI values were initially lower on
cycle day 2 before starting HMG (0.775 0.003 versus
0.790 0.003), started to decline earlier (cycle day 8 versus
cycle day 10), and were significantly lower on the day of
HCG (0.773 0.003 versus 0.790 0.003), compared to
non-pregnant cycles, but were no different on the day of
oocyte retrieval or embryo transfer. Bassil et al. (1995)
concluded that an RI value >0.79 before starting HMG was
associated with a poor uterine response, and suggested that
an increased dose of HMG might improve blood flow and
uterine receptability.
Levi-Setti et al. (1995) also measured mean (right and left)
uterine artery PI with a 6.5 MHz vaginal transducer, from 5
days before HCG administration until oocyte retrieval, in 87
IVF patients, 17 of whom had multiple cycles of treatment.
Three or more embryos were transferred in all cycles. The
number of patients with continuous waveforms was not
stated. During the first IVF cycle, the PI was significantly
lower from 4 days before HCG through retrieval in patients
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483
Table VIII. Studies of the relationship of uterine blood flow to endometrial thickness and pattern. See Table II for abbreviations
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
MDV
PI
S/D
ratio
x
x
RI
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
PI
RI
S/D
ratio
MDV
A = abdominal ultrasound; C = circadian rhythm also studied; E = relationship to oestrogen, progesterone, or ovulation induction
also studied; H = hyperstimulation syndrome also studied. See Table II for other abbreviations.
In the first study (Coulam et al., 1994), mean right and left
uterine artery PI and endometrial thickness and pattern were
measured by transvaginal ultrasound with a 5 MHz
transducer on the day of HCG administration in 41 IVF
cycles, on the day of progesterone administration in 20 donor
oocyte cycles, and the day of ovulation in 24 natural cycles
with transfer of cryopreserved embryos. The PI was
significantly lower in conception cycles (2.79) than in
non-conception cycles (3.50), for natural cycles with transfer
of cryopreserved embryos, but no significant differences
were found in IVF or oocyte donor cycles. The 95th centile
of PI in conception cycles was >3.3, similar to that reported
by Strohmer et al. (1991). There was no difference in
average endometrial thickness in conception and
non-conception cycles; however, no pregnancies occurred
when the thickness was <6 mm. Lack of a triple-layered
endometrial pattern was significantly associated with failure
of conception in donor oocyte cycles, but not in other cycles.
Unfortunately, the correlation of PI with endometrial
thickness and pattern was not analysed.
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485
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R.P.Dickey
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
MDV
PI
RI
S/D
ratio
x
x
(INF,LI,N,E)
Zaidi et al. (1995a) (INF,PCO)
(E,N,PCO)
Nargund et al. (1996)
Oyesanya et al. (1996)
Zaidi et al. (1996a)
x
x
E = relationship to oestrogen, progesterone and ovulation induction also studied; INF = infertility LI = luteal insufficiency; N = normal
cycle also studied; PCO = polycystic ovaries. See Table II for other abbreviations.
487
Wave
form
Flow
volume
TAMV,
TAMX
Vmax, PSV,
MPSV
MDV
PI
x
RI
x
x
x
x
x
x
S/D
ratio
C = relationship to crownrump length and chorionic sac diameter also studied; E = relationship to oestrogen, progesterone and ovulation
induction also studied; O = ovarian blood flow also measured; S = spiral artery also measured. See Table II for other abbreviations.
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R.P.Dickey
Figure 8. Uterine artery; total (right plus left) flow volume (A), mean cross-sectional area (B), mean time averaged maximum velocity (C), heart
rate (D), mean resistance index (E), and spiral artery resistance index (F). Mean (SE) filled symbols, smoothed curve open symbols. Reprinted
with permission from Dickey and Hower (1995a).
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Table XII. Analysis by covariance of the relative effects of uterine blood flow variables to
uterine artery blood flow volume, with gestational age, pulse rate, other uterine blood flow
variables, and subject as covariants. Data are expressed as F-values. Reprinted with permission from Dickey et al. (1995a)
Flow volume
Week 59
Week 1016
Significance
9.54
<0.001
9.77
<0.001
11.89
<0.001
5.58
<0.001
NS
Velocity
Cross-sectional area
Significance
Uterine artery RI
1.35
NS
1.32
Spiral artery RI
2.00
0.038
1.27
NS
Gestational age
0.80
NS
2.77
NS
Pulse rate
0.90
NS
1.16
NS
Table XIII. Analysis of covariance of the relative effects of serum oestradiol or progesterone on uterine blood flow variables in
early pregnancy with gestational age, subject, and oestrogen or progesterone as covariants. Data are expressed as F-values.
Signs are derived from multiple linear regression. Reprinted with permission from Dickey and Hower (1996)
Uterine artery
Spiral artery
Flow
volume
Average
velocity
Average
diameter
Pulsatility
index
Resistance
index
Pulsatility
index
Resistance
index
1.70a
0.87
1.94a
1.88a
2.49b
1.24
1.12
1.89a
2.05a
1.24
0.96
1.22
0.77
0.89
Oestradiol
0.36
1.71
1.03
1.53
1.07
0.40
0.30
Progesterone
2.23a
1.30
1.10
0.55
0.44
0.73
0.92
1.40
0.60
1.89a
1.23
1.72
1.24
1.37
1.05
1.41
0.99
1.23
0.96
0.49
0.65
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R.P.Dickey
Figure 9. Mean (SE) serum oestradiol-17 (A) and progesterone (B) after treatment with human menopausal gonadotrophin (HMG, ) or clomiphene citrate (CC, s), or spontaneous ovulation (). Reprinted with permission from Dickey and Hower (1995c).
Dickey and Hower (1995b) examined the relationship between recumbent uterine blood flow and average chorionic
sac diameter (CSD) and crownrump length (CRL) during
the first 16 gestational weeks in normal singleton pregnancies to determine whether differences in blood flow
could explain some of the variability that occurs in normal
human embryos in early pregnancy (Nishimura et al.,
1968; Rossavik et al., 1988; Dickey and Gasser, 1993;
Guirgus et al., 1993). During gestational weeks 5 through
12, CSD increased 12-fold and CRL increased 13-fold,
while mean total (right plus left) uterine artery blood flow
increased only ~3-fold. After adjustment for the effect of
gestational age and oestradiol, by multiple regression
analysis, CSD was negatively related to spiral artery PI and
RI, but not to uterine artery blood flow volume PI or RI.
CRL was positively related to uterine artery blood flow
volume and negatively related to uterine artery PI and RI.
The findings of a relationship between uterine artery resistance indices and CRL suggest that there may also be an
association between uterine blood flow and embryonic
growth and well-being during the first trimester. In late pregnancy, increased uterine artery resistance and impaired uterine blood flow are associated with intrauterine growth
retardation (Fleischer et al., 1986; Jacobson et al., 1990; Kay
et al., 1991; North et al., 1994). Thus, a lag in CSD or CRL
found using grey scale ultrasound in the first trimester may
be an indication that additional studies of uterine blood flow
need to be performed and, if abnormal, that efforts should be
directed towards improving blood flow.
493
Figure 10. Mean (SE) uterine artery total (right plus left) flow volume (A), mean diameter (B), mean time averaged maximum velocity (C) and
mean resistance index (D), following treatment with human menopausal gonadotrophin (HMG, ) or clomiphene citrate (CC, s), or spontaneous
ovulation (). Reprinted with permission from Dickey and Hower (1995c).
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495
Figure 11. Effect of standing (percentage change), mean (SE) on (A) ascending uterine artery [flow volume (UA-VOL, unbroken line), pulsatility
index (dashed line), resistance index (dotted line)] and (B) spiral artery [pulsatility index (dashed line), resistance index (dotted line)] in all subjects
(a), subjects with increased UA-VOL, (b), and subjects with decreased UA-VOL (c). Reprinted with permission from Dickey et al. (1994).
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Table XIV. Effect of standing on ascending uterine artery (UA) and spiral artery (SA) blood flow volume per minute (VOL), diameter (DIA), pulsatility index (PI) and resistance index (RI). Values are mean SE. Modified and reprinted with permission from
Dickey et al. (1994)
Recumbent
Value
Value
Value
126.2 6.6b
90.0
% Change
61.6
6.6
80.
10.9
12.8
142.8 9.1c
UA-DIA (mm)
2.78 0.06
2.70 0.05
97.6 2.0
2.76 0.05
UA-PI
2.76 0.14
2.50 0.11
89.8 3.4b
2.40 0.13
86.6 2.5c
UA-RI
0.90 0.02
0.86 0.02
96.3
0.85 0.02
94.8 1.4c
SA-PI
2.10 0.10
2.07 0.11
0.95 0.08
96.4 5.8
SA-RI
0.84 0.02
0.80 0.02
1.6a
102.5 6.7
96.2 2.8
0.81 0.02
100.0 2.5
97.4 4.3
Pulse rate
72.4
2.4
89.4
4.2
124.2 4.6c
91.1
5.0
126.4 6.0c
Mean BP
89.4
1.9
92.8
2.1
104.2 2.4
94.3
1.8
105.2 1.6+
57.6
4.5
50.5
4.4
78.9
6.6
UA-DIA (mm)
2.88 0.05
2.69 0.05
UA-PI
2.65 0.08
2.73 0.11
UA-RI
0.89 0.01
78.5 4.3c
94.1 1.5c
65.8 2.8c
2.65 0.04
92.8 1.5c
103.5 2.9
3.08 0.22
115.2 6.7a
0.90 0.01
101.5 1.1
0.90 0.06
102.0 1.2
2.06 0.09
109.0 5.2
SA-PI
1.95 0.08
2.05 0.09
108.2 4.8
SA-RI
0.83 0.02
0.82 0.02
99.6 2.4
0.81
0.02
98.4 2.4c
Pulse rate
75.4
1.5
91.1
2.2
122.3 2.7c
94.0
2.6
125.0 3.6c
Mean BP
91.4
1.0
93.5
1.3
102.7 1.4
96.1
1.6
105.3 1.6b
BP = blood pressure.
a,b,cPaired t-test, standing versus recumbent, 38 min versus 914 min: aP < 0.05, bP < 0.01, cP < 0.001.
497
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Conclusions
Doppler ultrasound measurement of uterine blood flow
holds the promise of being as helpful for investigation of
infertility and early pregnancy loss as Doppler analysis of
uterine and umbilical blood flow has been in the second
and third trimesters of pregnancy. This promise has not yet
been fulfilled, in part due to the difficulty of interpreting
blood flow measurements performed during the menstrual
cycle and early pregnancy when diastolic blood flow is
often not continuous in uterine and spiral arteries. Lack of
fulfilment is also due, in part, to the fact that most studies
have measured only downstream impedance, which is
critical in the second and third trimesters, but may not be as
499
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