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Sonographic and Doppler Sonographic Examination of Uterine Anomalies
Table 26.1 Intraoperative findings in 420 infertile women undergoing hysteroscopy
Findings Number of patients
Submucous leiomyoma 46
Endometrial polyp 35
Intrauterine adhesionsn 19*
Septate uterus 278
Arcuate uterus 28
Bicornuate uterus 16
Total 422
a
One patient with an endometrial polyp and one patient with intrauterine adhesions had a septate uterus.
b
Diagnosed by the combined use of laparoscopy and hysteroscopy.
With permission from Kupesic S, Kurjak A.: Septate uterus: detection and prediction of obstetrical complications by different forms of ultrasonography. J Ultrasound Med. 17 (1998) 631–636.
a
b
Blood flow in the septum and myometrium was assessed by
color and pulsed Doppler examination. Flow velocity
waveforms were sampled from all blood vessels that could be
26
visualized, and the resistance index (RI) was calculated.
Starting with the maximum frequency, the RI was calculated
by using the formula: (maximum systolic velocity–end-diastolic velocity) ⫼ maximum systolic velocity.
Hysterosonography. Each patient was placed in a gynecological examination chair for the intrauterine instillation of
isotonic saline solution. In a total of 76 patients, the cervix was
visualized with a speculum and swabbed with iodine solution.
A catheter with an outer diameter of 1.6mm and inner diameter of 1.1 mm was carefully inserted into the cervical canal. The
catheter cuff was inflated with 1.5–2ml of sterile saline to prevent leakage of the instille d fluid. From 10 to 20 ml of isotonic
saline solution was slowly injected with a syringe to distend
the uterine cavity. The speculum was then removed, and the
vaginal transducer was inserted. Scans in the transverse and
sagittal planes defined the septum as an echogenic structure
dividing the uterine cavity into two parts.
pendicular sectional planes were displayed simultaneously on
the monitor, permitting a detailed analysis of uterine morphology. Coronal scans were particularly helpful in diagnosing
the uterine anomaly.
Results
Table 26.2 reviews the sensitivity, specificity, and positive and
negative predictive values of transvaginal sonography, transvaginal color and pulsed Doppler, hysterosonography, and
three-dimensional ultrasound in the diagnosis of septate
uterus.
Transvaginal ultrasound. In 264 cases a presumptive diagnosis
of septate uterus was made on the basis of transvaginal Bmode findings. Fourteen patients had a false-negative diagno-
sis. Thus, the sensitivity of transvaginal sonography in the di-
agnosis of septate uterus was 94.96%.
Transvaginal color and pulsed Doppler ultrasound. A septate
uterus could be diagnosed in 276 cases by Doppler examination, corresponding to a sensitivity of 99.28%. A septate uterus
was incorrectly diagnosed in one patient with an endometrial
polyp and in another patient with intrauterine adhesions.
Thus, the reliability of Doppler sonography was decreased
when other intracavitary lesions such as an endometrial polyp
or submucous leiomyomas were present.
Color and pulsed Doppler examinations demonstrated a
septal blood supply in 198 of the patients (71.22%) (Fig. 26.
4).
262
Three-dimensional ultrasound. Eighty-six women undergoing
hysteroscopy were also examined by 3 D ultrasound. This was
preceded by a transvaginal B-mode, color Doppler and pulsed
Doppler examination. Hysterosonography was additionally
performed in 12 of these women. The examiner did not know
the results of the previous examinations. Three mutually per-
Table 26.2 Sensitivity, specificity, and positive (PPV) and negative predictive values (NPV) of various imaging procedures in the diagnosis of septate uterus in 420 patients with a history of infertility or spontaneous abortion
Imaging procedure Sensitivity (%) Specificity (%) PPV (%) NPV (%)
Transvaginal B-mode ultrasound 94.96 92.86 95.65 91.77
Transvaginal color and pulsed Doppler ultra-
sound
Hysterosonography 100.00 95.65 98.18 100.00
Three-dimensional ultrasound 93.55 96.55 98.31 87.50
With permission from Kupesic S, Kurjak A.: Septate uterus: detection and prediction of obstetrical complications by different forms of ultrasonography. J Ultrasound
Med. 17 (1998) 631–636.
99.28 99.30 99.64 98.60
Fig. 26.4 Transvaginal ultrasound image of a septate uterus. Two
separate endometrial compartments are visible during the proliferative phase of the cycle. Color Doppler demonstrates small myometrial
vessels in the septum.
Ultrasound in the Diagnosis and Treatment of Septate Uterus—Authors’ Results
The RI values in the septal vessels ranged from 0.68 to 1.0
(mean RI = 0.84 ⫾ 0.16) (Fig. 26.
detected in 18 patients, while continuous diastolic flow was
present in all the rest.
Hysterosonography. In 76 women, the intrauterine instillation
of isotonic saline solution was recommended prior to hysteroscopy. A clear-cut diagnosis of septate uterus was made in 54
(71.5 %) of the patients. The sensitivity and negative predictive
value of hysterosonography following transvaginal color
Doppler scanning were 100%. In one woman with dense intrauterine adhesions, however, the uterine septum could not
be detected even by hysterosonography.
5). No diastolic blood flow was
Three-dimensional ultrasound. Three-dimensional images of
good quality were obtained in 86 patients (Fig. 26.
6). The 3 D
ultrasound findings agreed with hysteroscopic findings in 58
patients with a septate uterus. However, an arcuate uterus was
diagnosed by 3 D ultrasound in four women who had a septate
uterus. The uterine cavity in these patients appeared to be
deformed by a fibroid in the fundal area. A false-positive diagnosis of septate uterus was made in one patient with intrauterine adhesions.
Radiographic hysterosalpingography. Radiographic HSG was
performed in 188 women during a 12-month period preceding
our study. A septate uterus was diagnosed in 49 of these
patients based on the Reutercriteria
23
. A septate uterus was as-
sumed to b e present when the angle between the two cavities
was ⬍ 75⬚, a bicornuate uterus when the angle was ⬎ 105⬚.In
15 cases (7.98%), hysterosalpingography showed a deformed
uterine cavity but no evidence of a congenital uterine anomaly.
The overall sensitivity of radiographic HSG in the diagnosis of
septate uterus was only 26.6 %.
Obstetric complications. In the second part of our five-year
study (1992–1996), we compared the obstetric complications
in 278 patients with a septate uterus with an average control
group. Early pregnancy loss occurred in 114 of the 278 patients
(41.1 %), compared with a 15% incidence in the control group.
Late abortions and preterm deliveries occurred in 35 of the 278
patients (12.59%), compared with 7% in the controls. Intrauterine growth retardation occurred in two pregnancies
with a septate uterus (8.7%), versus 6% in the controls. The incidence of intrauterine fetal death was 4.35% in our patients and
0.5% in our control group. Placental abruption was found in
one patient with a septate uterus (4.35 %), and placenta previa
was diagnosed in another patient (4.35 %). Breech presentation
occurred in six women with a septate uterus (26.9 %) and trans-
verse presentation in two (8.70%). Since septate uterus has a
significantly higher statistical association with abnormal fetal
presentations, the rate of cesarean sections was also significantly higher (34.78 %). Cervical insufficiency during preg-
Fig. 26.5 Same patient as in Fig. 26.4. Pulsed Doppler waveform
analysis shows a moderately high RI (0.69), which is typical of the
radial arteries.
Gynecological Ultrasound
Fig. 26.6 Three-dimensional ultrasound image of a septate uterus,
which shows a normal outer uterine contour and a thick septum extending into the uterine cavity.
nancy was documented in nine patients (25.71%) with a septate uterus.
Ectopic pregnancy was diagnosed in 76 of the patients
(27.34%), which was twice the incidence found in the control
group (13.3%). Seven patients with a septate uterus were found
to have bilateral ectopic pregnancies.
Follow-up after hysteroscopic surgery. We followed the reproductive outcomes in 116 patients (32 with primary infertility,
16 after one spontaneous abortion, 12 after preterm deliveries,
and 26 after recurrent abortions) who had undergone hysteroscopic surgery for an intrauterine septum. The prospective follow-up period was scheduled for 24 months in all patients. The
pregnancy rate in the study group was 50.86%: 44 patients
(74.58%) with term deliveries, 11 (18.64%) with first-trimester
abortion, and 4 (6.78%) with early pregnancy loss. The other
patients (162) were followed in the same way but for periods
less than 24 months, and so they are not reported in this study.
263
Sonographic and Doppler Sonographic Examination of Uterine Anomalies
New Thoughts on Old Problems
In the past, at least two diagnostic procedures have been
routinely used in the diagnosis of congenital uterine anomalies. The attending gynecologist should be aware, however,
that an extended diagnostic workup delays treatment, increases costs, and leads to greater risks and discomfort for the
patient
23
. Patients with a septate uterus require a prompt, accurate diagnosis as a prelude to surgical correction of their disorder.
Histology of the septal endometrium. Fedele et al.
7
that an intrauterine septum can be a cause of primar y infertility. When they examined the endometrial surface morphology
of biopsy samples taken in the preovulatory phase of the cycle,
they found significant structural differences between the septal endometrium and the endometrium of the lateral uterine
wall. These histological changes included a reduced number of
irregularly distributed glandular ostia, incomplete ciliogenesis
on ciliated cells, and a decreased ratio of ciliated to nonciliated
cells. These changes were indications that the differentiation
and estrogen-stimulated maturation of the septal en-
26
dometrium were irregular. Since the hormone levels in the
study patients were normal for cycle phase, the most plausible
hypothesisis that the mucosa covering the septum is poorly responsive to estrogens, perhaps because of deficient blood flow
to the septal connective tissue.
Muscle fiber content of the septum. March
16
believed that the
septum was composed of fibroelastic tissue, while Fayez
thought that it consisted mostly of connective tissue with a
small amount of muscle fib ers. Our study results could not confirm this. Color and pulsed Doppler ultrasound demonstrated
septal blood flow in 71.22 % of the patients, indicating that most
of the septa were supplied by myometrial vessels.
Dabirashrafi et al.
4
performed histological examinations of
uterine septa from 16 patients who underwent abdominal
metroplasty. Four uterine biopsies were taken from each
patient: one from the septum near the serosal layer, one from
the middle of the septum, one from the tip of the septum, and
one from the left posterior uterine wall. The authors found less
connective tissue in the septum (confirmed by the Bonferroni
criteria for multiple comparisons) and a greater average
amount of muscle tissue, muscle interlacing,and vesselswith a
muscle wall. These findings were contrary to the classic view
on the histological makeup of the intrauterine septum. The
small amount of connective tissue in the septum could be responsible for the poor decidual transformation and placentation that occur following implantation at this site
4, 5
. Also, the
greater amount of muscle tissue and interlaced muscle fibers
in the septum could lead to pregnancy loss as a result of increased or uncoordinated contractions.
showed
height of the uterine cavity and in patients whose septum occupied more than two-thirds of the uterine cavity. The same
correlation was found for septal thickness: obstetric complications were equally common in patients with thin and thick
septa (p ⬎ 0.05). The spontaneous abortion rate did show a significant correlation with septal blood flow, however. The
patients with a vascularized septum had a significantly higher
incidence of spontaneous abortions in early pregnancy and
complications in late pregnancy than the patients with a nonvascularized septum (p ⬍ 0.05).
Information gained with color Doppler. Uterine morphology,
including the endometrial layer and uterine musculature, can
be accurately evaluated with transvaginal ultrasound. Color
flow can simultaneously display the morphology and vascular
system of the uterus, supplying valuable information on the
nature and extent of uterine anomalies. Color Doppler contributes to evaluation of the myometrium by demonstrating
the myometrial vessels. Doppler can also be used to diagnose a
scant septal blood supply and/or inadequate development of
the endometrium in patients with a septate uterus
Uses of three-dimensional ultrasound. Three-dimensional ultrasound can provide uterine scans that accurately demonstrate the notch in the fundal region and the length of the intrauterine septum (Fig. 26.
7). In our experience, however, this
technique can give the false impression of an arcuate uterus in
5
patients who have a leiomyoma in the fundal region. This lesion imparts a concave shape to the uterine cavity, while the
dimple in the fundus appears indistinct. The value of 3 D ultrasound is also limited by acoustic shadows that are cast by
uterine fibroids, an irregular endometrial layer, and a small
uterine cavity (due to intrauterine adhesions).
Comments. Our study
15
showed conclusively that obstetric
complications are more common in patients with a septate
13, 14
.
264
Septal height, septal blood flow, and obstetric complications.
In a more recent study at our department
14
, no correlation was
found between the height of the intrauterine septum and the
occurrence of obstetric complications (p ⬎ 0.05). Abortions
and complications during late pregnancy had the same
frequency in patients with small septa less than one-third the
Fig. 26.7 Another three-dimensional ultrasound image of a septate
uterus. A thick septum subdivides the uterine cavity. The extent of the
anomaly is clearly defined.
References
uterus than in other women. In particular, ectopic pregnancy
was twice as common in these patients (27.34%) as in the con-
trol group (13.3%). A possible cause might be menstrual reflux,
which is common in women with uterine anomalies and may
impede the transport of the fertilized oocyte into the uterine
cavity. Our study clearly showed that patients with primary infertility or recurrent pregnancy problems benefited from surgical removal of the intrauterine septum.
In the conventional management of a septate uterus, inter-
vention is delayed until the first obstetric problem arises, since
a large percentage of patients have no complications
8
. But
given the higher infertility rates in women with a septate
uterus and the good results that can be achieved with endoscopic surgery, we are obliged to recommend hysteroscopy as
soon as we diagnose this condition, if possible even before the
patient conceives
12, 14, 15
. It appears that incision of the septum
can prevent implantation at an unfavorable site, either by re-
vascularization of the uterine connective tissue in the fundal
area or by suppressing uterine contractions that might expel
the pregnancy
7
. Since both events can be demonstrated with
color or pulsed Doppler ultrasound, this technique can be efficiently utilized both for the diagnosis of congenital anomalies
and for the follow-up of hysteroscopic surgery.
References
1 Ashton D, Amin HK, Richart RM, Neuwirth RS: The incidence of asymp-
tomatic uterine anomalies in women undergoing transcervical tubal
sterilization. Obstet. Gynecol. 72 (1988) 28–30
2 Cararach M, Penella J, Ubeda J, Iabastida R: Hysteroscopic incision of
the septate uterus: scissors versus resectoscope. Hum. Reprod. 9
(1994) 87–89
3 Carrington BM, Hricak M, Naruddin RN: Mullerian duct anomalies: MR
evaluation. Radiology 170 (1990) 715–720
4 Dabrashrafi H, Bahadori M, Mohammad K, Alavi M, Moghadami-Ta-
brizi N, Zandinejad R: Septate uterus: New idea on the histologic features of the septum in this abnormal uterus. Amer. J. Obstet. Gynecol.
172 (1995) 105–107
5 Fayez JA: Comparison between abdominal and hysteroscopic metro-
plasty. Obstet. Gynecol. 68 (1986) 399–403
6 Fedele L, Arcaini L, Parazzini F, Vercellini P, Nola GD: Metroplastic hys-
teroscopy and fertility. Fertil. Steril. 59 (1993) 768–770
7 Fedele L, Bianchi S, Marchini M, Franchi D, TozziL, Dorta M: Ultrastruc-
tural aspects of endometrium in infertile women with septate uterus.
Fertil. Steril. 65 (1996) 750–752
8 Gaucherand P, Awada A, Rudigoz RC, Dargent D: Obstetrical prognosis
of septate uterus: a plea for treatment of the septum. Eur. J. Obstet. Gynecol. Reprod. Biol. 54 (1994) 109–112
9 Goldenberg M, Sivan E, Sharabi Z: Reproductive outcome following
hysteroscopic management of intrauterine septum and adhesions.
Hum. Reprod. 10 (1995) 2663–2665
10 Heinonen PK, Saarikoski S, Pystynen P: Reproductive performance of
women with uterine anomalies. An evaluation of 182 cases. Acta Obstet. Gynecol. Scand. 61 (1982) 157–162
11 Jurkovic D, Giepel A, Gurboeck K, Jauniaux E, Natucci M, Campbell S:
Three dimensional ultrasound for the assessment of uterine anatomy
and detection of congenital anomalies: a comparison with hysterosalpingography and two-dimensional sonography. Ultrasound Obstet.
Gynecol. 5 (1995) 233–237
12 Keltz MD; Olive DL, Kim AH, Arici A: Sonohysterography for screening
in recurrent pregnancy loss. Fertil. Steril. 67 (1997) 670–674
13 Kupesic S, Kurjak A: Uterine and ovarian perfusion during the peri-
ovulatory period assessed by transvaginal color Doppler. Fertil. Steril.
3 (1993) 439–443
14 Kupesic S, Kurjak A: Comparison of B-mode, color Doppler, threedi-
mensional ultrasound and hysterosonography in detection of septate
uteri. Am. J. Obstet. Gynecol. (1998)
15 Kupesic S, Kurjak A: Pregnancy after diagnosis and treatment of ute-
rine anomalies. Croat Med. J. (1998)
16 March CM: Hysteroscopy as an aid to diagnosis in female infertility.
Clin. Obstet. Gynecol. 26 (1983) 302–312
17 Marshall C, Mintz DI, Thickman D, Gussman H, Kressel Y.: MR evalua-
tion of uterine anomalies. Radiology 148 (1987) 287–289
18 McShane PM, Reilly RJ, Schiff L: Pregnancy outcome following Tomp-
kins metroplasty. Fertil. Steril. 40 (1983) 190–194
19 Nicolini U, Bellotti B, Bonazzi D, Zamberleti G, Battista C: Can ultra-
sound be used to screen uterine malformation? Fertil. Steril. 47 (1987)
89–93
20 Randolph J, Ying Y, Maier D, Schmidt C, Riddick D: Comparison of real
time ultrasonography, hysterosalpingography, and laparoscopy/hysteroscopy in the evaluation of uterine abnormalities and tubal
patency. Fertil. Steril. 5 (1986) 828–832
21 Reuter KL, Daly DC, Cohen SM: Septate versus bicornuate uteri: errors
in imaging diagnosis. Radiology 172 (1989) 749–752
22 Richman TS, Viscomi GN, Cherney AD, Polan A: Fallopian tubal patency
assessment by ultrasound following fluid injection. Radiology 152
(1984) 507–510
23 Salle B, Sergeant P, Galcherand P,Guimont I, De Saint Hilaire P, Rudigoz
RC: Transvaginal hysterosonographic evaluation of septate uteri: a
preliminary report. Hum. Reprod. 11 (1996) 1004–1007
24 Sorensen S: Estimated prevalence of mulerian anomalies. Acta Obstet.
Gynecol. Scand. 67 (1988) 441–445
25 Taylor PJ, Cumming DC: Hysteroscopy in 100 patients. Fertil. Steril. 31
(1979) 301–304
26 ValdesC, Malini S, Malinak LR: Ultrasound evaluation of female genital
(1984) 285–290
Gynecological Ultrasound
265
Doppler Examination of the Normal Endometrium and
27
Benign Endometrial Changes
S. Kupesic and A. Kurjak
Changes in the Normal Endometrium during the Menstrual Cycle
The endometrium appears sonographically as a central, echogenic layer in the uterine wall. Its structural details are clearly
defined by transvaginal imaging
of the endometrium depend upon the plasma levels of circulating estrogens and progestins.
Menstrual phase. During menstruation in the healthy, fertile
woman, the two functional layers of the endometrium (the
stratum compactum and spongiosum) are shed
the stratum basale, from which the endometrium is re-
27
generated. Hormone withdrawal and the changes in the spiral
arteries are key components of this mechanism. Increased coiling of the spiral arteries leads to an arrest of circulation, which
in turn causes progressive tissue ischemia. Vasoconstriction of
the spiral arteries and necrosis of their vessel walls finally lead
to menstrual bleeding
times visible with ultrasound reflect this structural breakdown
of the endometrium. As the menstrual phase progresses, both
hypoechoic areas (blood) and hyperechoic areas (sloughed endometrium) can be seen. As menstruation ends, the endometrium appears sonographically as a thin, almost linear,
slightly irregular echogenic layer.
Early follicular phase. The endometrium is normally less than
5 mm thick in the early follicular phase. The endometrial
24
. The hypoechoic areas that are some-
6
. The thickness and structure
36
, leaving only
glands, lined by relatively flat cells, are now almost tubular. Mitoses become more numerous, and blood vessels grow from
the stratum basale toward the endometrial surface, where a
capillary network is formed. At this time the endometrium appears sonographically as a hyperechoic layer. In some cases it
cannot be clearly distinguished from the myometrium.
Ovulation. The endometrial glands are even more numerous
around the time of ovulation, and the endometrial thickness
averages 10 mm. A three-layered endometrial structure is typical of the follicular phase. The hyperechoic structure of the
endomyometrial junction is most conspicuous at this time.
Secretory phase. This phase is characterized by a marked increase in glycogens, acid phosphatases, and lipids in the endometrium. The endometrium appears uniformly hyperechoic, losing its three-layered structure and hypoechoic
border. During this phase of the cycle, the endometrium appears markedly hyperechoic to the myometrium.
Midluteal phase. The endometrium shows its greatest
sonodensity in the midluteal phase, when it appears uniformly
hyperechoic. Posterior acoustic enhancement is typical of this
phase of the cycle.
266
Changes in Endometrial Blood Flow during the Menstrual Cycle
Transvaginal color and pulsed Doppler ultrasound can b e used
to examine endometrial perfusion under normal and pathological conditions.
Comparison of normal and stimulated cycles. The increase in
endometrial blood flow during the course of the menstrual
cycle is based on the blood flow changes that occur in the
uterine, arcuate and radial arteries (Fig. 27.
occur in the flow velocity waveforms of the spiral arteries
during the normal ovulatory cycle have been tracked with
Doppler ultrasound
sistance index (RI) is equal to 0.54 ⫾ 0.03 (Fig. 27.
blood flow velocity begins to rise. The RI reaches its lowest
point (0.49 ⫾ 0.05) between days 16 and 18 of the cycle. In the
stimulated cycle, by contrast, the resistance rises on the last
day before ovulation. It may be that the induction of ovulation
evokes this uterine response, which should be evaluated with
26
. On the day before ovulation, the re-
1). The changes that
2) and the
Fig. 27.1 Transvaginal scan of the uterine vascular supply: uterine ar-
teries at the level of the corpus–cervix junction, arcuate arteries encircling the uterus, and radial arteries within the myometrium.
Fig. 27.2 Color Doppler signals from the periphery of the multilayer
endometrium. Increased blood flow velocity and a decreased resistance index (RI = 0.55) are noted on the day of ovulation.
Changes in Endometrial Blood Flow during the Menstrual Cycle
blood flow, intraendometrial vascular penetration, and subendometrial blood flow velocity on the day of hCG administration and
related the results to pregnancy rates. The overall pregnancy rate
was 32.3%. There was no significant difference between the pregnant and nonpregnant groups in terms of endometrial thickness,
subendometrial peak systolic flow velocity V
pulsatility index (PI). The pregnancy rates based on endometrial
morphology were not significantly different: 17.6% for type A (hyperechoic) endometrium, 33.3% for type B (isoechoic), and 35.6%
for type C (three-layered). In eight patients, subendometrial blood
flow and intraendometrial vascularization were not detected. When
endometrial blood flow was not detected, implantation did not
occur.The pregnancy rates related to the depth of vascular penetra-
tion into the endometrial and subendometrial regions were 26.7%
for the subendometrial region (zone 1), 36.4 % for the outer hyperechoic region (zone 2), and 37.9% for the inner hyperechoic region
(zone 3), but the differences were not statistically significant. Of the
cycles with type A endometrium, 23.5 % showed no subendometrial
color flow. This was greater than the frequency of absent color flow
noted in the type C endometrium.
, or subendometrial
max
Doppler scans prior to embryo transfer. Endometrial blood
flow appears to provide a noninvasive parameter that is better
for predicting uterine receptivity than the flow velocity in the
uterine artery. Analysis of the blood flow changes in the spiral
arteries should be used in predicting successful implantation,
investigating unexplained fertility problems, and referring
patients with abnormal endometrial blood flow for appropriate treatment
25
(Table 27.1).
Comparison of the normal cycle and luteal insufficiency. Our
most recent study
uterine, spiral, and radial vessels decreases at the transition from
the follicular to the luteal phase in women with normal endometrial
development. But in patients with delayed endometrial development and luteal insufficiency, rising uterine vascular resistance is
measured during the course of the luteal phase. In women with a
luteal phase defect, the impedance values in the spiral arteries were
increased in the preovulatory phase (RI = 0.70 ⫾ 0.06, p ⬍ 0.001),
midluteal phase (RI = 0.72 ⫾ 0.01, p ⬍ 0.001), and late luteal phase
(RI = 0.72 ⫾ 0.04, p ⬍ 0.001). Because the most significant devia-
27
has clearly shown that flow resistance in the
tions from normal impedance values in the intraovarian and sub-
Zaidi et al.46recently published interesting data on this subject.
They examined 96 women in an IVF program on the day of human
chorionic gonadotropin (hCG) administration by transvaginal color
Doppler sonography. They assessed endometrial thickness and
morphology, the presence or absence of intra- and subendometrial
endometrial vessels were seen in patients with luteal insufficiency,
we may conclude that color and pulsed Doppler ultrasound is help-
ful in the assessment of luteal phase adequacy. Moreover, Doppler
ultrasound can be used along with, or even in place of, hormonal
and histological markers in the evaluation of uterine receptivity.
Table 27.1 Blood flow in the spiral arteries during the preovulatory phase
Time from ovulation (days) Maximum systolic blood flow velocity
Resistance index Pulsatility index
(cm/s)
–3 6.21 ⫾ 0.0 4 0.55 ⫾ 0.02 0.86 ⫾ 0.05
–2 6.02 ⫾ 0.09 0.54 ⫾ 0.03 0.85 ⫾ 0.09
–1 6.32 ⫾ 0.12 0.48 ⫾ 0.04 0.83 ⫾ 0.12
0 6.68 ⫾ 0.68 0.48 ⫾ 0.06 0.84 ⫾ 0.14
+ 1 7.46 ⫾1.31 0.49 ⫾ 0.05 0.72 ⫾ 0.12
Gynecological Ultrasound
With permission from Kupesic S, Kurjak A: Uterine and ovarian perfusion during the periovulatory period assessed by transvaginal color Doppler. Fertil. Steril. 60
(1993) 439–443.
267
Doppler Examination of the Normal Endometrium and Benign Endometrial Changes
Submucous Leiomyomas
The uterine fibroid is one of the most common tumors that
occur in the lesser pelvis of women during their reproductive
45
years
. Leiomyomas may be intramural, submucous, or subserous, and some are pedunculated. The clinical hallmarks of
submucous leiomyomas are metrorrhagia, pain in the lesser
pelvis, or infertility. The presence and severity of the symptoms depend largely on the number, size, and location of the
tumors. The ultrasound diagnosis of leiomyoma is based on a
change in uterine contour, uterine enlargement, and/or a
change in echo texture.
Detection by transvaginal sonography and hysteroscopy. Because the proportions of smooth muscle and connective tissue
in leiomyomas are highly variable, these benign tumors vary
greatly in their sonographic appearance from hypoechoic to
hyperechoic. As a result, they are occasionally misinterpreted
as endometrial polyps, blood, or mucus. Fedele et al.
the accuracy of transvaginal sonography in the detection of
small submucous myomas in patients who underwent transvaginal sonography and hysteroscopy before a scheduled hys-
27
terectomy. The sensitivity of transvaginal sonography was
100%, its specificity was 94%, the positive predictive value of an
14
tested
abnormal finding was 81%, and the positive predictive value of
an abnormal examination was 100%. These figures are comparable to the values reported for hysteroscopy (100%, 96 %,
87 %, and 100%, respectively). Transvaginal ultrasound is more
accurate than hysteroscopy in the localization of leiomyomas
but is less accurate in distinguishing between a leiomyomaand
an endometrial polyp.
Leiomyomas and infertility. The relationship between leio-
myomas and infertility or habitual abortion is still poorly
understood. Many women with leiomyomas can conceive
without difficulty and carry their pregnancy to term. On the
other hand, pregnancy rates of 10–89% have been reported in
previously infertile patients who had their fibroids removed
43
The cause of fibroid-associated infertility is still unknown,
however. It has been theorized that the tumors may decrease
the area available for implantation, decrease the contractility
of the uterine musculature, cause venous changes in the endometrium, or obstruct the cervix and fallopian tubes, causing
interference with sperm transport.
Vascularization of uterine leiomyomas. With transvaginal and
color Doppler sonography, it is possible to measure blood flow
in small vessels and also to obtain more reproducible measure-
31
ments
(Table 27.2).
.
Fig. 27.3 Submucous leiomyoma, delineated by its increased vascularity. The color flow signals map the rich vascular supply at the tumor
base.
Kurjak et al.31examined 161 women: 101 patients with palpable
uterine fibroids and 60 healthy volunteers. Flow velocity waveforms
were used to analyze the vascular resistance in the uterine arteries
and in the main arteries supplying the definable fibroids. Color flow
signals were detected at the periphery of the tumors and also at
their center (Fig. 27.3). Diastolic flow was always detectable in these
vessels and was usually greater than in the uterine arter y. The mean
RI of myometrial blood flow was 0.54, and the mean pulsatility
index (PI) was 0.89 (Fig. 27.4). All of the tumors were benign on his-
tological examination, even when the RI was very low. Low RI values
were found in necrotic tumors and in tumors with secondary
degenerative or inflammatory changes. Examination of the uterine
arteries in the control group showed a mean RI of 0.84 and a PI of
2.525. Significantly lower values were measured in the fibroid
group: 0.74 for RI and 1.65 for PI. The flow velocity, RI, and PI were
each measured between the 5th and 8th days of the menstrual
cycle.
Table 27.2 Uterine artery blood flow parameters in patients with palpable (vascularized) uterine fibroids and in healthy volunteers
Blood flow parameter
Control group
(n = 60)
Patients with
vascularized
fibroids (n = 81)
268
Fig. 27.4 Same patient as in Fig. 27.3. Analysis of the flow velocity
waveform (right) indicates moderate vascular resistance (RI = 0.54).
Velocity (cm/s) 34.4 ⫾ 12.25 47.08 ⫾ 18.46
Resistance index (RI) 0.84 ⫾ 0.09 0.74 ⫾ 0.09
Pulsatility index (PI) 2.52 ⫾ 0.87 1.65 ⫾ 0.49
With permission from Kurjak A, Kupesic S, Miric D: The assessment of benign
uterine tumor vascularization by transvaginal color Doppler. Ultrasound Med.
Biol. 18 (1992) 645–649.
Endometrial Polyps
The results of this study show that the vascularization of a
tumor depends largely on its size and location and on the extent of secondary degenerative changes. Large, laterally situated myomas, especially those with necrotic, degenerative,
and inflammatory changes, usually show increased diastolic
flow and a decreased resistance index (RI
min
= 0.35).
Myomas during pregnancy. Other factors in addition to size
should be considered in the sonographic evaluation of myomas: their location, their spatial relationship to the placenta,
their echogenicity
12
, and their Doppler values23. A significantly
increased incidence of threatened abortion, premature labor,
placental abruption, and lower abdominal pain was observed
in patients with myomas (p ⬍ 0.001)
was most common with myomas larger than 200 cm
12
. Placental abruption
3
, sub-
mucous myomas, and myomas located under the placenta.
Kessler et al.23showed that conventional ultrasound was unable to
distinguish between a myoma and local thickening of the uterine
wall due to a transient contraction. In such cases, repeat scanning
Endometrial Polyps
approximately 30 min later was able to differentiate contractions,
which usually resolved, from myomas. The authors examined 10
patients using B-mode and color Doppler sonography. In five
patients with myomas, they observed splaying of the vessels
around the tumor, whereas in five patients with contractions, there
was no vascular displacement in the area of local myometrial thickening. Thus, color Doppler sonography can help eliminate the need
for a prolonged ultrasound examination in questionable cases.
RU 486 and leuprolide acetate. Reinisch et al.37studied the ef-
fect of RU 486 and leuprolide acetate on uterine artery blood
flow and uterine volume in patients with myomas. Uterine
artery blood flow declined steadily in the patients receiving RU
486, showing a 40% decrease. The patients who received leuprolide acetate showed a 21% decrease. Both groups also
showed a significant decrease in uterine volume at three
months. It was assumed that the reduction in uterine artery
blood flow provided the mechanism for the decrease in uterine
size and for the decreased uterine blood loss at the time of
surgery or hysteroscopy.
Gynecological Ultrasound
Because flow resistance is markedly decreased in and around
endometrial polyps, an inexperienced examiner might mistake these lesions for a uterine malignancy. Endometrial pol-
yps are best demonstrated in the early proliferative phase or
following the injection of a “negative contrast medium” into
the uterine cavity.
Histology and blood supply. Endometrial polyps may be single
or multiple, occur in pedunculated and various other forms,
and are often composed of hyperplastic basalis tissue
16, 32
. Almost two-thirds contain no functional endometrium, and
many show the histological features of cystic hyperplasia. They
derive their blood supply from preexisting terminal branches
of the uterine arteries. Blood flow can be demonstrated in multiple separate vessels, and the blood flow velocity can b e analyzed (Table 27.
tected, and the RI is usually higher than 0.45
3, Fig. 27.5). Diastolic flow can always be de-
30, 32
(Fig. 27.6). The
RI tends to be lower in polyps with necrotic and inflammatory
changes (RI
= 0.37). Polypoid structures may appear in infer-
min
tile women on GnRH (gonadotropin-releasing hormone) therapy but usually disappear in the next cycle if in-vitro fertilization was unsuccessful.
Fig. 27.5 An oblique scan in a premenopausal patient shows a demarcated zone of increased echogenicity, typical of an endometrial
polyp. The normally branching vessels are well defined.
Table 27.3 Vascularization of benign uterine changes
Type of uterine change Number RI
Submucous leiomyoma 38 0.54 ⫾ 0.06
Adenomyosis 62 0.57 ⫾ 0.08
Endometritis 28 0.50 ⫾ 0.06
Incomplete abortion 31 0.41 ⫾ 0.02
Endometrial polyp 46 ⬎ 0.45
Fig. 27.6 Same patient as in Fig. 27.5. Analysis of the flow velocity
waveform (right) shows a high resistance index (0.69), which is typical
of an endometrial polyp.
269
Doppler Examination of the Normal Endometrium and Benign Endometrial Changes
Tamoxifen and incidence of endometrial polyps. Tamoxifen is a
nonsteroidal antiestrogen widely used in the hormonal treatment of breast cancer. Studies are currently under way to determine whether it could also be used in healthy women at increased risk for breast cancer. The weak estrogen-like action of
tamoxifen on the endometrium calls for vigilance in the management of these cases. Since several studies have reported endometrial carcinomas during tamoxifen use, patients receiving
tamoxifen should be regularly examined. A number of pathological changes have been described during long-term tamoxifen use (20 mg/day)
20
, including epithelial metaplasia, simple
and atypical hyperplasia, endometrial polyps, and endometrial
carcinoma
1
. Endometrial changes present sonographically as
abnormal endometrial thickening and nonhomogeneous increased echogenicity with numerous small cystic lesions. At
least three studies have linked tamoxifen therapy in postmenopausal breast cancer patients to a high incidence of endometrial polyps
3, 13, 35
. Achiron et al.3found that 44% of these
patients had a conspicuous “honeycomb-like” endometrial
structure on B-mode ultrasound, which was associated with a
correspondingly high occurrence (40%) of endometrial polyps.
On the other hand, two large studies in postmenopausal
women on tamoxifen therapy showed no cor relation between
27
an endometrial thickness ⬎5 mm and abnormal endometrial
findings
8, 44
.
Tamoxifen and endometrial blood flow. So far, little research
has been done on the effect of tamoxifen on endometrial blood
2
flow. Achiron et al.
described blood flow changes in the endometrium and subendometrial regions. On examining
asymptomatic, postmenopausal women with an endometrial
thickness ⬍5 mm who were taking tamoxifen, these authors
found increased endometrial blood flow with a significant fall
of RI compared with an untreated control group. Another study
by the same authors
1
showed a markedly lower RI in women
with endometrial thickening, especially in the presence of endometrial polyps, than in women with a normal endometrium
(mean value of 0.39 vs. 0.79). After the endometrial polyps
were removed, the RI values returned to normal, supporting
the notion of a benign, transitory effect of long-term tamoxifen
therapy on the endometrium.
Endometrial adenofibromas. Huang et al.
19
described two
cases of endometrial adenofibroma that occurred during prolonged tamoxifen use. Adenofibromas are rare, benign, mixed
mesodermal tumors. Their sonographic appearance differs
from that of endometrial polyps, endometrial hyperplasia, and
endometrial carcinoma and more closely resembles the
“snowstorm” appearance of trophoblastic disease (hydatidiform mole). They can be differentiated with color and pulsed
Doppler ultrasound: lacunae with turbulent blood flow are
characteristic of trophoblastic diseases, whereas low-resistance blood flow is suggestive of endometrial adenof ibroma.
270
Endometrial Hyperplasia
The endometrial echo in postmenopausal women generally
appears simply as a linear echo 1–3 mm thick. The thickness of
the echo is increased in association with certain benign uterine
changes such as endometrial hyperplasia. An endometrial
thickness ⬎14mm in premenopausal women and ⬎5mm in
postmenopausal women warrants further investigation
peak incidence of adenomatous hyperplasia is between 40 and
50 years of age.
Fig. 27.7 Thickened endometrium (10 mm) in an asymptomatic
postmenopausal woman. Note the peripheral arrangement of the ves-
sels and the moderate RI of 0.54, which is typical of endometrial hyper-
plasia.
32
. The
Differentiation from endometrial carcinoma. Benign and
malignant changes cannot be differentiated by their morphology alone, and so transvaginal B-mode scanning is not
sufficient to distinguish hyperplasia from carcinoma. Both hyperplasia and carcinoma display typical vascular structures,
however, and therefore they can be detected with sensitive
Doppler instruments
16, 30
. Branches from normal vessels extending into the peripheral part of the endometrium form a
typical pattern seen with hyperplasia (Fig. 27.
7). On Doppler
examination, blood flow signals are usually recorded from the
periphery of the hyperplastic endometrium (Table 27.
3). Sig-
nificant differences in RI values have been discovered between
endometrial carcinoma (mean RI = 0.42) and endometrial hyperplasia (mean RI = 0.50)
28
(Figs. 27.8,27.9). Some clinicians
have already begun to consider sonographic and Doppler parameters when selecting patients for biopsy or observation.
This appears to be particularly advantageous in older patients
in poor general health and in patients with cervical stenosis.
Gredmark et al.
17
found that 15% of women with postmenopausal bleeding had adenomatous hyperplasia or endometrial carcinoma, while 50% were found to have an
atrophic endometrium. This suggests that ultrasound and
Doppler sonography should be included in the workup of postmenopausal bleeding, both to avoid the unnecessary biopsy of
atrophic endometrium and to disclose any ovarian abnormalities that may be present.
Kurjak et al.
33
reported that endometrial carcinomas could
be detected even in asymptomatic women by noninvasive
Adenomyosis
Fig. 27.8 Peripheral neovascularization of endometrial carcinoma,
demonstrated by color Doppler.
transvaginal color and pulsed Doppler sonography and that
this method could even be used for screening.
Sheth, however, found an overlap of PI and RI values between
benign and malignant causes of endometrial thickening
39
. Endometrial arterial flow was seen in 23 of 36 (64 %) benign endometrial lesions. The mean RI was 0.48 ⫾ 0.13 (range 0.27–0.84)
while the mean PI was 0.72 ⫾ 0.33 (0.31–1.77). Abnormal vascularity was found in 56% of endometrial carcinomas. The mean PI in this
group was 0.71 ⫾ 0.32 (0.42–1.17), while the mean RI values were
the same as for the benign lesions: 0.48 ⫾ 0.15 (0.34–0.69).
Adenomyosis
Adenomyosis has been found in 10–50% of autopsy series and
in 5.6–61.5% of surgical specimens
characterized by an ingrowth of endometrial tissue into the
myometrium.This tissue may directly adjoin the endometrium
or it may deeply penetrate the myometriumand even reach the
serosa.
Sonographic and clinical characteristics. Most patients with
adenomyosis have either a normal-sized uterus or nonspecific
uterine enlargement
4
. Ultrasound typically shows a diffusely
enlarged uterus with a thickened myometrium that has a
“Swiss cheese” appearance due to blood and tissue collections
in the muscle
40
(Fig. 29.10). Severe cases generally show an unsettled echo pattern in the central endometrial layer. Occasionally the entire uterus is hypoechoic, but large cysts are
rarely found. The typical symptoms of adenomyosis include
dysmenorrhea, lower abdominal pain, and menometrorrhagia.
Dysmenorrhea is caused by bleeding from the endometrial
tissue within the myometrium. Hysterosalpingography occasionally shows the passage of contrast material into the myometrium.
Role of color Doppler. Fedele et al.
dovaginal ultrasound in the diagnosis of diffuse adenomyosis.
Sensitivity and specificity were 80 % and 74%. With color Doppler sonography and spectral analysis, it is possible to examine
the uterine blood flow in adenomyosis and compare it with
34, 38
. Uterine adenomyosis is
15
tested the value of en-
Fig. 27.9 The Doppler waveform indicates a low RI (0.34), which is
typical of endometrial carcinoma.
Chan et al.7found that transvaginal sonography was superior
to color Doppler imaging in the detection of endometrial
pathology, but neither method could distinguish benign from
malignant lesions. By contrast, Bonilla-Musoles et al.
5
found a
positive correlation between uterine artery resistance values
and the likelihood of carcinoma in postmenopausal women.
Based on the positive correlation between arterial flow resistance and time in years since menopause
29
, it should be
possible to estimate the cancer risk in postmenopausal women
who show decreased vascular resistance.
uterine blood flow in other benign conditions
31, 34
. The authors
found that the mean RI of blood flow in the myometrium
reached 0.56, while the uterine artery RI was decreased (0.75)
compared with healthy volunteers (0.87). The differences between leiomyomas and adenomyosis are explained partly by
the fact that leiomyomas have a higher estrogen receptor density than the surrounding myometrium. As a result, leiomyomas are responsive to changes in the luteal hormone level,
whereas adenomyosis is marked by a deficiency of estrogen
and progesterone receptors
10
.
Differentiation from uterine malignancy. Hirai et al.18evaluated
44 benign uterine masses and seven uterine malignancies to determine whether Doppler sonography was useful in differentiating adenomyosis from uterine malignancies. For this purpose they used
an adenomyosis score based on the parameters of myometrial
thickness, structure, contour, and also Doppler findings. The RI
values tended to be lower for malignant lesions (mean RI = 0.40 ⫾
0.07) than for adenomyosis (mean RI = 0.57 ⫾ 0.08). The latter
value also corresponded to the mean RI for leiomyomas (0.57). The
maximum blood flow velocity V
than for adenomyosis. The V
was higher for malignant lesions
max
in leiomyomas was only slightly
max
higher than in adenomyosis. Thus, statistically significant differences were found between malignant neoplasms and adenomyosis
for RI and for V
. A slight difference in V
max
was found between ad-
max
enomyosis and leiomyomas, but there was no difference in RI.
Gynecological Ultrasound
271