Abstract
Doppler ultrasound imaging can be used to identify and assess blood vessels by producing a colour-coded map of Doppler shifts superimposed on a B-mode ultrasound image. The effect, first described by the Austrian scientist Christian Doppler in the middle of the nineteenth century, has been used to provide information regarding blood flow in ultrasound’s daily practice in the last five to six decades. Blood flow in arteries and veins can be recorded from the surface of the skin, allowing flow analysis in systole and diastole, in both normal and diseased blood vessels. Over time, Doppler techniques became an important technique in diagnostic ultrasound for haemodynamic assessment, replacing some invasive procedures in many clinical situations.
Introduction
Doppler ultrasound imaging can be used to identify and assess blood vessels by producing a colour-coded map of Doppler shifts superimposed on a B-mode ultrasound image. The effect, first described by the Austrian scientist Christian Doppler in the middle of the nineteenth century, has been used to provide information regarding blood flow in ultrasound’s daily practice in the last five to six decades. Blood flow in arteries and veins can be recorded from the surface of the skin, allowing flow analysis in systole and diastole, in both normal and diseased blood vessels. Over time, Doppler techniques became an important technique in diagnostic ultrasound for haemodynamic assessment, replacing some invasive procedures in many clinical situations [1,2].
This chapter aims to describe the use of Doppler ultrasound in gynaecology, the most important Doppler settings in gynaecology and its role in diagnosing normal and pathological findings.
Doppler Settings
Blood flow can be detected and visualized by colour, power and pulse wave Doppler. While pulse wave Doppler is widely used in obstetrics, colour and power Doppler give us essential information in gynaecology. With the help of colour Doppler, colour pixels with Doppler frequency shift are visualized and colour content in a structure can be subjectively assessed. Colour Doppler offers also the possibility to identify the direction of flow. In power Doppler – also referred to as energy Doppler, amplitude Doppler or Doppler angiography – the energy of backscattered ultrasound waves with changed frequency is displayed. It is mandatory to take into account that in order to detect Doppler signals, the correct Doppler settings are essential. In gynaecology, blood vessels with low velocities are examined and assessed – therefore, Doppler settings are different from those used in obstetrics.
In daily practice the ultrasound examiner needs to ‘calibrate his/her brain’ to the quality of the ultrasound system (Doppler technique sensitivity) and will make many changes to the controls and try different probe positions to optimize the image [3]. Factors affecting Doppler ultrasound image are: Doppler gain, power, frequency, pulse repetition frequency (PRF), wall motion filter (WMF), Doppler persistence, angle of insonation, distance between transducer and the vessels, the size of region of interest and density of red blood corpuscles. These Doppler settings and factors affecting Doppler ultrasound examination have to be taken into account for each patient. Out of these, the three most important Doppler settings are PRF, WMF and gain. In gynaecology, we suggest using low PRF (0.3–0.6 kHz) and low WMF to avoid missing low-velocity flows. For adjusting the gain, we suggest using the sub-noise technique. Briefly, the sub-noise gain is obtained by increasing gain until noise artefacts are visible, then reducing it until the artefacts just disappear [4].
Uterus: Changes through the Menstrual Cycle
Vascularization of the endometrium changes every month because of physiological angiogenesis in women with natural menstrual cycles. In 3D power Doppler ultrasound studies, endometrial vascularization was found to increase during the follicular phase and reach a maximum two or three days before ovulation, and thereafter decrease dramatically 2–5 days after ovulation and then increase progressively during the remaining luteal phase [5,6]. Low vascularization in the endometrium directly after ovulation might be important for endometrial receptivity and angiogenesis. In postmenopausal women, normal endometrium is thin (≤4 mm) and no blood flow in the endometrium is detected using Doppler ultrasound [7].
Infertility
Tubal Patency
Increasing interest has been given to ultrasound evaluation of subfertile women and a thorough investigation of infertility factors is proposed by performing a single ultrasound scan between days 5 and 9 of the menstrual cycle: the ‘one-stop shop’ approach [8]. As part of this comprehensive strategy, tubal patency status is usually assessed by injecting echogenic contrast media (air + saline in hystero-contrast sono-salpingography (HyCoSy); foam in hystero-salpingo-foam sonography (HyFoSy)) into the uterine cavity [9].
Doppler and 3D ultrasound can be used as complementary tools for investigating tubal patency, enhancing diagnostic accuracy [9]. During 2D/3D ultrasound scan with a vaginal probe, power Doppler is turned on simultaneously with foam injection in a transverse/coronal view of the uterus at the level of the uterine horns; this is the 2D/3D Doppler HyFoSy technique [10] (Figure 16.1). A pervious tube creates a positive flow next to the uterine lateral wall, suggesting free movement of the contrast media along the tubal lumen. A positive flow has been recently described as the ‘flaming-tubes’ sign [10], and it is helpful to improve the reliability of tubal patency testing [11].
Endometrial Receptivity for Embryo Transfer
Some reports have suggested that Doppler, particularly 3D power Doppler quantification, could be useful to predict outcomes after embryo transfer as higher pregnancy and lower miscarriage rates would occur in a highly vascular endometrium; in such a scenario, spectral Doppler would help identify an endometrium with lower resistance or higher vascularization indices and select the ideal cycle for embryo transfer [12–16].
However, conflicting results [12,17], high heterogeneity among study designs and variables measured [14], small numbers of patients included [17] and low reproducibility and high dependency on machine settings [18] still represent major limitations, and the evaluation of endometrial vascularization by Doppler ultrasound is still considered a very limited tool for assessing endometrial receptivity [19].
Benign Uterine Pathology
The use of Doppler ultrasound in assessing the endometrium and uterine cavity shows good performance in differentiating benign from malignant endometrial lesions [20,21]. The endometrial pathologies are different in their vascularization, and Doppler ultrasound helps to identify blood vessels in different lesions.
Endometrial Hyperplasia
Endometrial hyperplasia is a condition that might be suspected at ultrasound examination. The morphological appearance of the endometrium with endometrial hyperplasia with and without atypia overlaps. The progression of atypical hyperplasia to endometrial cancer might be observed in up to 28 per cent of cases, which increases the importance of its early detection [22]. When using colour and power Doppler, in the case of endometrial hyperplasia disordered vessels may be seen (Figure 16.2), while the presence of multiple vessels with focal origin may be associated with endometrial cancer.
Multifocal vascularization at the endometrial–myometrial junction is related to non-specific findings, including atrophic endometrium, secretory or proliferative endometritis.
Endometrial Polyp
Most endometrial polyps are benign; however, 1–4 per cent of polyps may be malignant [23,24]. Several factors are related to the increased risk of endometrial cancer, such as age, overweight, diabetes, hypertension, Lynch syndrome and polycystic ovary syndrome. There is a strong relationship between the presence of a feeding vessel (a pedicle artery) and the diagnosis of polyp, with a specificity of 98 per cent and a positive predictive value of 96 per cent [25] (Figure 16.3). The presence of a single dominant vessel, a ‘pedicle artery’, with or without branching, in the Doppler study decreases the risk of malignant lesion. However, pedicle artery is observed in only 24 per cent of the polyps in postmenopausal women [7].
(a) Retroverted uterus, thick endometrium and ‘pedicle artery’, endometrial polyp is suspected
(b) intrauterine focal lesion is clearly visible during saline sonohysterography. The histology showed benign endometrial polyp.
Myoma
Uterine myoma is a common benign gynaecological condition, affecting about 25 per cent of women. Myomas are usually well-defined lesions [26]. A typical myoma has a circumferential or intralesional blood flow pattern [27,28] (Figure 16.4). The vascular patterns of myomas and focal adenomyosis (adenomyomas) are different and colour and power Doppler ultrasound may help in discriminating these pathologies.
Adenomyosis
Adenomyosis can be diagnosed using greyscale ultrasound [28–30]; however, histological examination of the uterus specimen is still the gold standard. Focal adenomyosis (adenomyoma) might simulate a myoma on greyscale ultrasound examination. In the case of focal adenomyosis, the lesion is ill-defined and has translesional flow, i.e. blood vessels are perpendicular to the uterine cavity/serosa crossing the lesion [28].
Malignant Uterine Pathology
Endometrial Cancer
Transvaginal ultrasound examination helps to discriminate between benign and malignant endometrial lesions. Irregular echogenicity of the endometrium at greyscale ultrasound examination gives us a suspicion of malignancy. Irregular echogenicity together with higher vascularization of endometrium at colour and power Doppler ultrasound, irregular branching of blood vessels, dense areas of the vessels and colour splashes increase risk of endometrial malignancy [31–33] (Figure 16.5).
Uterine Sarcoma
Uterine sarcoma is usually a single, large tumour. It may mimic a benign myoma or in some cases appear as a large tumour with irregular vascularization and sometimes necrotic areas [34,35] (Figure 16.6). There is very scarce information on the role of greyscale and Doppler ultrasound in differentiating benign myomas from sarcomas and most of the studies are small, retrospective case series.
(a) Endometrial sarcoma – 30-year-old woman with menometrorrhagia. Ultrasound shows a rounded lesion in the uterine cavity with multifocal vessels. Diagnosis was made after hysteroscopy and resection.
(b,c) Leiomyosarcoma: a 45-year-old woman with irregular bleeding. Ultrasound shows a heterogeneous single large mass with increased vascularization.
Ovary
Normal Ovary
Ovarian angiogenesis is a required condition for the early stages of folliculogenesis and growth of the corpus luteum. Vascular supply in the ovary may play an important role in the growth and differentiation of the follicles and in the selection of the dominant follicle [36,37]. In premenopausal women with natural menstrual cycles, vascularization of the dominant ovary and dominant follicle increases during the follicular phase and continues to increase after ovulation, being higher during the luteal than follicular phase, while no changes in vascularization occur in the non-dominant ovary [38]. At the end of the luteal phase, vascularization of the corpus luteum decreases physiologically.
Colour and power Doppler ultrasound can help in identifying corpus luteum as this physiological lesion typically presents abundant peripheral blood vessels, surrounding it as a thin rim: the ‘ring of fire’ sign [39] (Figure 16.7). Colour and power Doppler ultrasound allow for differentiating the corpus luteum from other adnexal masses, i.e. endometriomas, and helps to confirm ovulation in infertility patients monitored by serial transvaginal sonography in natural or stimulated cycles [40].
It has been suggested that blood flow in the corpus luteum is closely related to its function, and significant changes are observed during the menstrual cycle [41,42] and pregnancy [43]. However, the diagnostic role of spectral Doppler is no longer considered useful [44]. Ovaries in postmenopausal women are small; the size of the ovaries is similar regardless of the number of years in menopause, and colour Doppler signals may be detected in only about two-thirds of ovaries [45].
Ovarian Torsion
Ovarian torsion is one of the reasons for acute pelvic pain. Signs of ovarian torsion at transvaginal greyscale ultrasound examination are enlarged ovary, oedematous stroma, loss of follicular content or peripheral cysts, solid appearance or abnormal position of the ovary. When using colour and power Doppler, a twisted ovarian pedicle (‘whirlpool sign’) may be seen. There may be reduced or absent arterial flow; however, normal Doppler findings do not exclude ovarian torsion (Figure 16.8).
Benign Ovarian Pathology
New vessel formation is essential in growth of benign ovarian cysts, malignant tissue growth and metastasis to the ovaries. Tumour vascular morphology and biological behaviour differ from normal vasculature [46]. Vascularization of ovarian pathology can be assessed using colour and power Doppler ultrasound. Colour content in the tissue can be estimated subjectively or objectively. The International Ovarian Tumor Analysis (IOTA) group suggested colour score in estimating vascularization in the lesion: colour score 1 = no vascularization; colour score 2 = only minimal flow detected; colour score 3 = moderate flow present; colour score 4 = richly vascularized lesion [47]. Good intra- and interobserver agreement for the colour score has been observed [3]. Objective quantification of blood flow using spectral Doppler has been shown to fail in discriminating between benign and malignant ovarian lesions. 3D power Doppler ultrasound vascular indices have been found to add little to a correct diagnosis of malignancy in the ordinary tumour population [48].
Specific ultrasound diagnosis in the majority of ovarian cysts can be made by using pattern recognition on greyscale ultrasound and subjective assessment of the colour content in the lesion contributes little to the specific diagnosis [49,50]. High diagnostic accuracy of transvaginal ultrasound is described in diagnosing endometriomas with sensitivity and specificity of over 90 per cent, particularly among women aged up to 35 years [51]. Similarly, a cystic ovarian mass with detectable flow within an internal papillary projection is seen in only 2.5 per cent of histologically confirmed endometriomas and in 30 per cent of confirmed malignant ovarian masses [52,53]. However, vascularization in endometriomas may vary widely, from absent detectable blood flow to moderate or abundant vascularization; therefore, Doppler ultrasound adds little in confirming the diagnosis of endometriomas [52] (Figure 16.9).
(a) Typical endometrioma – unilocular cyst with ground glass echogenicity
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