The Veterinary Journal 197 (2013) 205–210

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The Veterinary Journal

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Uterine artery blood flow characteristics assessed during oestrus and

the early luteal phase of pregnant and non-pregnant bitches
S.L. Freeman a, M. Russo b, G.C.W. England a,⇑
a
Division of Veterinary Surgery, School of Veterinary Medicine and Science, Faculty of Medicine and Health Sciences, University of Nottingham, Sutton Bonington Campus,
Leicestershire LE12 5RD, UK
b
Obstetric Unit, Department of Veterinary Clinical Sciences, Veterinary School, University of Naples, Napoli, Italy

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to measure uterine artery blood velocity daily using Doppler ultrasonography
Accepted 15 February 2013 in 10 young and 10 older clinically normal bitches throughout oestrus.
Typical arterial waveforms identified in young bitches were characterised by a systolic peak and sub-
sequent flow throughout diastole, whereas in older bitches, flow was sometimes absent in diastole. For
Keywords: 3 days immediately prior to ovulation, at the time of declining plasma oestrogen and increasing proges-
Bitch terone concentrations, resistance index (RI) increased, principally associated with decreased diastolic
Blood flow
velocity; in some bitches there was absent late diastolic flow during this time. In older bitches, the wave-
Fertility
Perfusion characteristics
form appearance was more variable, with absent late and early diastolic flow observed in some cases.
Uterine artery Mean RI was higher throughout oestrus for older bitches compared with young bitches, although both
groups had a similar 3-day duration increase before ovulation. Nine of the young bitches and five of
the older bitches became pregnant; litter size was smaller for the older bitches. Non-pregnant bitches:
(1) were significantly older; (2) had fewer waveforms with continuous diastolic flow 2 days before ovu-
lation; (3) had lower end diastolic velocity, higher RI and fewer waveforms with continuous diastolic flow
2 days after ovulation, and (4) had lower plasma progesterone concentrations 5 days after ovulation.
These are the first detailed observations of uterine artery blood velocity and waveform appearance
throughout oestrus in bitches, and this is the first description of a link between impaired diastolic flow
and reduced fertility. Assessment of uterine artery velocity could be useful to promote understanding
of physiological mechanisms and could also become an important tool to assess potential infertility.
Ó 2013 Elsevier Ltd. All rights reserved.

Introduction 1998, 2000, 2003). A crucial association between the time-aver-

Doppler ultrasonography has been used for the evaluation of
uterine artery blood flow in a number of species, including women
and mares (Goswamy and Steptoe, 1988; Bollwein et al., 1998,
2000, 2002). Common assessments of the uterine artery include
measurement of peak systolic velocity (PSV) and end diastolic
blood velocity (EDV), as well as calculation of blood flow volume
or average velocity. Although useful, these calculations might be
flawed, especially when vessel size is very small and when the
Doppler angle and machine gain are not consistent (Dickey,
1997). However, calculation of resistance index (RI) is not subject
to these errors and as a simple ratio of the PSV and EDV, it forms
a useful estimation of downstream impedance to blood flow and
therefore the degree of uterine perfusion.
Fluctuations in uterine artery blood flow have been related to
stage of the oestrous cycle in cows and mares (Bollwein et al.,
⇑ Corresponding author. Tel.: +44 115 9516411.
E-mail address: gary.england@nottingham.ac.uk (G.C.W. England).
aged maximum blood velocity and the uterine nitric oxide
synthase (NOS) system has been established; it is likely an oestro-
gen-mediated stimulation of NOS (Honnens et al., 2011). Important
variations in uterine artery RI have been documented, associated
with age and parity in women and mares (Dickey, 1997; Bollwein
et al., 1998; Ousey et al., 2012) and as part of an increased uterine
perfusion following mating (Bollwein et al., 2003). Doppler ultra-
sound examination of the uterine artery is common in human
pregnancy since there is an association between blood flow param-
eters and adverse fetal outcome (Dickey, 1997; Iacovella et al.,
2012). Interesting observations have been made between de-
creased uterine perfusion during the menstrual cycle and human
infertility (Goswamy et al., 1988; Kurjak et al., 1991; Steer et al.,
1994), and although recent work suggests limited association be-
tween these parameters (Kim et al., 2010), the initial studies of
Goswamy et al. (1988) did not just make flow-associated measure-
ments, rather, they devised descriptive criteria for classification of
the waveforms, and suggested that these were valuable estimates
of blood flow. Despite those early observations, analysis of
waveform characteristics is rarely performed because it is not

1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.tvjl.2013.02.015
206 S.L. Freeman et al. / The Veterinary Journal 197 (2013) 205–210
amenable to evaluation by ultrasound machine software, and as a
result it is often omitted from clinical investigation of infertility
(Dickey, 1997). Despite this, there has recently been increasing
interest in the relationship between ultrasound-measured endo-
metrial blood flow and infertility (Ng et al., 2007).
In the bitch, measurement of the uterine artery blood flow with
Doppler ultrasound has been reported in non-cycling and pregnant
animals (Alvarez-Clau and Liste, 2005), and recently interesting
physiological changes have been documented after the deposition
of semen into the uterus (England et al., 2012b) and in cases of
endometrial disease (England et al., 2012a). However, to the
authors’ knowledge, there are no published studies of the variation
of uterine artery blood flow in bitches during oestrus, and investi-
gations of any possible associations with age, parity, or fertility
have not previously been reported.
We hypothesise that in the bitch there are fluctuations of uter-
ine artery blood flow and waveform characteristics during oestrus,
and that these could differ according to age and might be associ-
ated with reduced likelihood of establishing a pregnancy.
Materials and methods
Ethical approval
All procedures were conducted as part of normal veterinary clinical practice
with owner permission and the ethical approval of the School of Veterinary Medi-
cine and Science, University of Nottingham.
Animals
Twenty Labrador retriever bitches that were presented for monitoring of oes-
trus to determine the optimal time for natural mating were used for the study.
The bitches were mated to one of 12 different Labrador retriever dogs that had
all been fertile within the previous 3 months. Semen samples were collected from
all male dogs between 5 and 7 days after the last mating. Ejaculates were separated
using glass funnels into pre-sperm, sperm-rich and prostatic fractions. The sperm-
rich fractions were evaluated for volume, motility, concentration and morphology
(Pacey et al., 2000) to enable calculation of the total number of normal live sperma-
tozoa per ejaculate.
Bitches were divided into two groups of 10 designated as ‘young’ (aged 28–
38 months) and ‘older’ (aged 50–68 months). Five of the young bitches and all of
the older bitches had previously been pregnant; the remaining five young bitches
had not previously been mated. All pregnancies had been approximately 1 year pre-
viously and none of the bitches had been mated at the preceding oestrous cycle.
Each bitch had a normal clinical reproductive tract examination, including normal
uterine ultrasonography at the onset of proestrus.
Bitches were examined daily for collection of vaginal epithelial cells and cyto-
logical examination was performed after staining with a Romanowsky stain (Diff
Quik) to establish the anuclear cell index (Moxon et al., 2010), and for measurement
of plasma concentrations of progesterone by ELISA (Ridgeway Science). Approxi-
mately 90 min before vaginal cytology was performed, the bitch was placed into left
lateral recumbency and the uterine arteries were located using trans-abdominal B-
mode ultrasonography with a 10 MHz mechanical sector transducer (Pie-Data UK,
Ltd.). The transducer was placed on the ventral abdomen in the transverse imaging
plane with an incident angle of approximately 45°. The uterine artery (positioned
lateral to the uterine vein) was detected adjacent to the mid uterine body and
was confirmed using the colour Doppler setting. Using pulsed-Doppler, a small
sample gate was placed over the artery and minor positional adjustments were
made to facilitate recording of uterine artery waveforms. The waveforms were
examined subjectively and classified as defined by Goswamy and Steptoe (1988)
and modified by Dickey et al. (1994): Type C was a systolic peak followed by the
diastolic wave continuous with systole and extending throughout the remainder
of the cardiac cycle to the next systole; Type A was a systolic peak with absence
of the early diastolic wave, but with flow present in mid and late diastole; Type B
was a systolic peak followed by the diastolic wave continuous with systole but
not extending to the next systole (i.e. there was no flow in late diastole), and Type
D was a systolic peak with absence of the early and late diastolic wave, but with
flow present in mid diastole. Other waveform profiles reported in women (Gosw-
amy and Steptoe, 1988; Dickey, 1997) were not identified in preliminary studies
(data not shown) and so no further classification categories were assigned. Mea-
surements were made of PSV and EDV; in cases of Type B and Type A waveforms,
the latest diastolic velocity before the decline to baseline was measured. RI was cal-
culated using the formula:
RI ¼ ðPSV  EDVÞ=PSV
Measurements were made from three waveforms each from the left and right
uterine artery.
Mating occurred 1 day after plasma progesterone concentrations exceeded
5 ng/mL (designated as the day of ovulation, day 0) and a second mating was per-
formed 48 h later. The owners of the dogs provided pregnancy and whelping data.
Statistical methods
Means were calculated and the differences between time periods within treat-
ments (young or older bitches) were analysed using a two-way analysis of variance
and Tukey’s post hoc test, while differences between treatments (young and older
bitches) for each time period were analysed using the Mann Whitney U test. Data
were then re-classified according to the pregnancy outcome (pregnant or non-preg-
nant) and were compared between the pregnant and non-pregnant groups for days
2 and +2 in relation to ovulation, and day +5 for plasma progesterone, using either
the Mann Whitney U test or chi-squared test with Yates correction. Analysis was
performed with InStat3 (GraphPad) and data were considered statistically signifi-
cant when P < 0.05.
Results
Each of the bitches had an apparently normal oestrous cycle,
ovulated and was mated. Semen quality was within the following
ranges: % normal motility, 70–85%; total live normal spermatozoa,
510–880  106 per ejaculate.
It was possible to identify the uterine arteries in all bitches and
at least three suitable waveforms were recorded at each examina-
tion. Each waveform had a characteristic appearance with high
systolic flow and an obvious diastolic wave. All four of the wave-
form classifications were identified at various times during the
study (Fig. 1). Since statistical analysis did not demonstrate signif-
icant differences between values for PSV, EDV and RI of the left and
right arteries, all six daily waveform measurements for each bitch
were pooled for subsequent evaluation.
For young bitches, there was a significant difference in RI across
the days of the study. RI values were lowest and not significantly
different to each other on days 5 to 3 and days +1 to +5, and
were significantly higher on days 2 to 0, respectively (Fig. 2a).
The change in RI was predominantly associated with a decrease
in EDV, which was significantly lower on days 2 to 0 compared
to all other days. There were no significant differences in PSV
across any of the days, although values were numerically higher
on days 2 to 0. Higher RI values corresponded with the graphi-
cally-identified trough in the peak of anuclear vaginal epithelial
cells at the time of the initial rise of plasma progesterone
(Fig. 2a). Examination of the waveform classification for the young
bitches showed that eight bitches had Type C waveforms through-
out the study, while two bitches had a Type C waveform on days
5 to 2, and days 0 to +5 inclusive, with Type B waveform on
day 1. Nine of the young bitches became pregnant with a mean
(±SD) litter size of 6.2 ± 1.8 pups.
For the older bitches, values for RI were significantly higher
than the young bitches for each day of the oestrous cycle
(Fig. 2b). Higher RI values were associated with lower EDV values;
PSV was not different between the two groups. The older bitches
had a similar trend in RI throughout the cycle as the young bitches;
there was a significant increase in RI on days 2 to 0, associated
with significantly lower values for EDV on these days. The subjec-
tive relationship between RI and the peak of anuclear vaginal epi-
thelial cells and first detection of a rise in plasma progesterone
concentration was similar for the older and young bitches
(Fig. 2b). RI returned to lower values on day +1, similar to the
young bitches (Fig. 2b). Examination of the waveform characteris-
tics for the older bitches showed that two of the bitches had a Type
C waveform on each day of the study. Of the remaining eight
bitches, four had Type C waveforms on days 5 to 3 and days
+3 to +5 inclusive and Type B waveforms on days 2 to +2, while
three bitches had Type C waveforms on days 5 to 3, and days
 S.L. Freeman et al. / The Veterinary Journal 197 (2013) 205–210 207

Fig. 1. Pulsed-wave Doppler ultrasound waveform characteristics from the uterine artery of three different bitches during oestrus. The x-axis represents blood velocity in m/s
and the y-axis is time in s. (a) Type C waveform: A systolic peak followed by a diastolic wave continuous with systole and extending throughout the remainder of the cardiac
cycle to the next systole. (b) Type A waveform: A systolic peak followed by absence of the early diastolic wave but with flow through mid and late diastole until the next
systole. (c) Type B waveform: A systolic peak followed by a diastolic wave continuous with systole but with absent late diastolic flow. (d) Type D waveform: A systolic peak
with absence of the early and late diastolic wave, but with flow present in mid diastole.

3 to +5 inclusive, and Type A waveforms on days 2 to +2. Finally,
one bitch had Type B waveforms on days 5 to 3 and days +3 to
+5 inclusive and Type D waveforms on days 2 to +2, respectively.
None of the latter three bitches became pregnant. Overall five of
the older bitches became pregnant with a mean (±SD) litter size
of 4.6 ± 1.1 pups.
Examination of progesterone concentrations showed that val-
ues were significantly higher on each day after the day of calcu-
lated ovulation for the younger bitches than the older bitches
(Figs. 2a and 2b).
Analysis of data after reclassification of the bitches into
pregnant (n = 14) and non-pregnant (n = 6) groups showed that
208 S.L. Freeman et al. / The Veterinary Journal 197 (2013) 205–210

Fig. 2a. Boxplot of resistance index of the left and right uterine artery, mean (±SE) plasma progesterone concentration (ng/mL; solid line) and mean (±SE) vaginal epithelial
cell anuclear index (%; dotted line), in relation to the estimated day of ovulation in 10 young Labrador bitches. Values between days with a letter in common, and
progesterone values between treatments (Figs. 2a and 2b; young and older, respectively) with a number in common are not significantly different (P > 0.05).

Fig. 2b. Boxplot of resistance index of the left and right uterine artery, mean (± SE) plasma progesterone concentration (ng/mL; solid line) and mean (±SE) vaginal epithelial
cell anuclear index (%; dotted line), in relation to the estimated day of ovulation in 10 older Labrador bitches. Values between days with a letter in common, and values
between treatments (Figs. 2a and 2b; young and older, respectively) with a number in common are not significantly different (P > 0.05).

compared with the pregnant bitches, the non-pregnant bitches: (1)
were significantly older; (2) had fewer Type C waveforms on day
2; (3) had lower EDV, higher RI, fewer Type C and more Type A
waveforms on day +2, and (4) had lower plasma progesterone on
day +5 (Table 1). Other parameters including post-mating semen
quality of the males was not different between pregnant and
non-pregnant bitches.
Discussion
In a number of species, study of uterine artery blood flow has
illuminated interesting physiological variations and highlighted
important biological consequences, particularly a link between re-
duced uterine perfusion and both infertility and early pregnancy
failure (Goswamy and Steptoe, 1988; Sterzik et al., 1989; Kurjak
et al., 1991; Ziegler et al., 1999; Iacovella et al., 2012). There has
been limited investigation of uterine blood flow in the bitch and
this study provides the first observation of changes in uterine ar-
tery blood velocity and RI throughout oestrus, as well as suggesting
a link between reduced perfusion (evidenced by absent early or
early and late diastolic flow), and failure to establish pregnancy.
In this study, baseline values during oestrus for PSV, EDV and RI
were similar to those reported previously in oestrous bitches (Eng-
land et al., 2012b) and early pregnant bitches (Di Salvo et al., 2006).
 S.L. Freeman et al. / The Veterinary Journal 197 (2013) 205–210 209

Table 1
Comparison of mean animal age, left and right uterine artery mean peak systolic velocity (PSV), mean end diastolic velocity (EDV), resistance index (RI), and arterial waveform
characteristics at 2 days before (day 2) and at 2 days after (day +2) ovulation, and mean plasma progesterone concentration on day 5 after ovulation for 14 pregnant and six non-
pregnant Labrador bitches. Post-mating mean total number of live normal spermatozoa for the two groups are also shown.

Parameter Pregnant Non-pregnant Statistical significance

(n = 14) (n = 6)
Mean age (±SD) (months) 39.8 ± 11.1 53.3 ± 12.8 P = 0.038
Day 2 flow measurements
Mean (±SD) PSV (cm/s) 28.4 ± 3.8 29.6 ± 3.1 NSD
Mean (±SD) EDV (cm/s) 9.2 ± 1.3 8.5 ± 1.8 NSD
Mean (±SD) RI 0.67 ± 0.05 0.71 ± 0.04 NSD
Day 2 waveform characteristics
Number (%) Type C waveforms 11 (78.6%) 1 (16.7%) P = 0.036
Number (%) Type B waveforms 2 (14.2%) 3 (50.0%) NSD
Number (%) Type A waveforms 1 (7.1%) 1 (16.6%) NSD
Number (%) Type D waveforms 0 1 (16.6%) NSD
Day +2 flow measurements
Mean (±SD) PSV (cm/s) 28.3 ± 4.1 28.6 ± 3.6 NSD
Mean (±SD) EDV (cm/s) 11.6 ± 1.8 10.0 ± 2.5 P = 0.04
Mean (±SD) RI 0.58 ± 0.07 0.65 ± 0.05 P = 0.034
Day +2 waveform characteristics
Number (%) Type C waveforms 11 (78.6%) 1 (16.7%) P = 0.036
Number (%) Type B waveforms 2 (14.2%) 0 NSD
Number (%) Type A waveforms 1 (7.1%) 4 (66.7%) P = 0.024
Number (%) Type D waveforms 0 1 (16.6%) NSD
Mean (±SD) plasma progesterone concentration on day +5 (ng/mL) 16.6 ± 1.4 14.3 ± 2.6 P = 0.026
Mean total number of live normal spermatozoa (106/ejaculate) 604.9 ± 180.5 671.6 ± 122.1 NSD
collected 5–7 days after mating

NSD, no significant difference.

There was an interesting short-duration increase in RI, indicating
decreased perfusion, which occurred over the 3 days prior to ovu-
lation at the time of the presumptive decrease in plasma oestrogen
(which occurs after the first peak of vaginal epithelial cells; Eng-
land, 1992), during the increase of plasma progesterone. A similar
decrease in uterine perfusion has also been observed at the time of
declining oestrogen concentrations in women (Goswamy and Step-
toe, 1988; Ziegler et al., 1999), mares (Bollwein et al., 1998) and
cows (Bollwein et al., 2000). We hypothesise that this change in
perfusion is associated with the withdrawal of the direct effects
of oestrogen on vascular smooth muscle (which normally induces
vasodilation; Scott et al., 2007). Unfortunately, our studies did
not examine uterine artery flow in these bitches during late anoes-
trus or proestrus, and therefore it is not clear whether baseline
uterine perfusion had already increased during the transition from
anoestrus to the follicular phase, when, at least in other species,
there is neo-angiogenesis associated with increasing plasma oest-
rogen concentrations (Foresta et al., 2010). Further studies are war-
ranted to investigate this, although previous work has shown
almost absent diastolic flow in anoestrous bitches (Alvarez-Clau
and Liste, 2005).
An important finding in the present study was lower EDV in
older bitches, resulting in higher values for RI on all days of the
cycle. RI has been shown to increase in older mares (Bollwein
et al., 1998; Ousey et al., 2012), presumably as a result of uterine
disease. In this study, all of the older bitches were of proven fer-
tility and had no ultrasonographic signs of endometrial hyperpla-
sia. Previous work has demonstrated higher RI in bitches with
endometrial hyperplasia detected by ultrasound (England et al.,
2012a). We postulate that the older bitches in the present study
had uterine changes that were not evident at the resolution pro-
vided by the ultrasound machine, and we suggest that future
studies might attempt to correlate uterine artery flow with histo-
logical appearance of the uterus. Despite being included in the
study because of a recent previous pregnancy, fewer older bitches
became pregnant, and mean litter size was smaller than for the
young bitches.
Examination of the appearance of the uterine artery waveforms
for the young bitches demonstrated that for the majority there was
continuous flow throughout diastole, with only two of the 10
bitches exhibiting early and mid, but not late, diastolic flow on a
few days of the cycle. In women, these two waveforms are consid-
ered to represent good uterine perfusion (Goswamy and Steptoe,
1988; Dickey, 1997). Interestingly, six of the older bitches had a
similar pattern, with predominately continuous diastolic flow
throughout all days of the cycle, or early and mid but not late dia-
stolic flow at the time that RI increased. In three older bitches that
did not become pregnant, there was a more variable pattern
including an absence of flow in both early and late diastole. Ab-
sence of early and late diastolic flow in women has been associated
with poor uterine perfusion and reduced fertility (Goswamy et al.,
1988; Kurjak et al., 1991).
Older bitches had lower concentrations of progesterone after
ovulation than younger bitches and, for those that became preg-
nant, litter size was smaller than for the young bitches. It is possi-
ble that in older bitches there were fewer follicles and corpora
lutea than in young bitches. This contention would need to be con-
firmed using careful ultrasound examination of the ovaries, and
although this was not performed in the present study, it would
be interesting to perform in groups of younger and older bitches,
since smaller litter size in older bitches has an uncertain aetiology
(Blythe and England, 1993).
Although only small numbers of animals were available for this
study, comparisons of the pregnant and non-pregnant groups dem-
onstrated that non-pregnant bitches were significantly older and
had lower plasma progesterone concentrations after ovulation
than the pregnant bitches. Examination of the uterine artery wave-
forms demonstrated that more of the non-pregnant bitches had an
absence of early and early and late diastolic flow than pregnant
bitches; furthermore, these bitches had lower EDV and higher RI.
Lower diastolic velocity, higher RI and absence of flow in diastole
indicates poor perfusion of the downstream vascular bed; presum-
ably in these bitches there was reduced ability of capillary vessels
to remain fully patent throughout diastole. This could have
210 S.L. Freeman et al. / The Veterinary Journal 197 (2013) 205–210
affected fertility potential in a variety of ways: (1) interfering with
normal changes in perfusion that occur at the time of mating; (2)
persisting into pregnancy and interfering with vascular develop-
ment of the placenta, or (3) some other undetermined mechanism.
In human reproduction, both former hypotheses appear important,
since increased RI and absence of flow at the beginning of diastole
during the menstrual cycle might result in infertility (Goswamy
and Steptoe, 1988; Sterzik et al., 1989; Kurjak et al., 1991; Ziegler
et al., 1999), while poor diastolic flow after fertilisation could result
pregnancy loss (Iacovella et al., 2012). Abnormal uterine artery
flow has not yet been reported in cases of canine pregnancy failure,
but clearly additional studies are warranted in bitches with abnor-
mal uterine artery waveforms during oestrus, to establish wave-
form characteristics during pregnancy and to elucidate whether
pregnancy outcome is affected.
Conclusions
The present study demonstrates important physiological
changes of uterine artery blood flow during oestrus of bitches,
and documents how perfusion and perfusion patterns might be re-
duced with age and could potentially impact fertility. The present
studies provide a foundation for further investigation in the bitch.
Conflict of interest statement
None of the authors have any financial or personal relationships
with other people or organisations that could inappropriately
influence or bias the content of this work.
Acknowledgements
The study received no funding from external bodies.
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