J Clin Ultrasound 18:227-234, May 1990
Transvaginal Color Doppler Imaging Asim Kurjak, MD, PhD, Davor Jurkovic, MD, Zarko Alfirevic, MD, and Ivica Zalud, MD
Abstract: Transvaginal color Doppler was used to assess circulation in pelvic vessels in a group of 64 patients including 15 patients with fertility problems, 18 patients with pelvic tumors, 2 cases of suspected ectopic pregnancy, and 29 pregnant patients with fetuses between 6 weeks and 10 weeks, menstrual age. Blood flow was successfully displayed by color Doppler in the external and internal iliac arteries, and the uterine atreries, but flow in ovarian arteries could not be visualized. In the subgroup of patients with pelvic tumors, neovascularization of tumor tissue was documented in 6 out of 10 cases of uterine fibroma and in 2 cases of ovarian cancer. In 6 cases involving benign ovarian pathology, no abnormal blood supply was observed. A comparison between the characteristics of blood flow within uterine fibromas and ovarian malignancies showed lower impedance and higher blood velocity in cases of malignancy. In early pregnancy blood flow in the umbilical artery could be visualized by color Doppler starting from the 6th week and flow in the aorta from the 8th week. Flow in the trophoblasts was observed with an overall success rate of 59% and successfully demonstrated in 1 out of 2 cases of ectopic pregnancy. Indexing Words: Doppler color imaging * Color imaging Transvaginal imaging
The most exciting recent developments in the field of diagnostic ultrasonography in obstetric and gynecology are, undoubtedly, color Doppler and transvaginal sonography.1-6 Color Doppler, or more precisely color-encoded real-time two-dimensional Doppler, imaging systems display flow as multiple points in a two-dimensional plane superimposed on a two-dimensional ultrasound image. The technique is based mainly on the moving target identification principle, which is, in fact, an autocorrelation techn i q ~ eA . ~delay line is used to bring data from subsequent images to a multiplier and the rate at which analogous signals are digitized in the scan converter provides continuous information on flow velocity. In the majority of commercially available units, flow toward the transducer is encoded in red, and flow going away from the transducer is encoded in blue. Flow velocity is proportional to the color brightness. Turbulence From the Ultrasonic Institute, University of Zagreb, WHO Collaborating Centre for Diagnostic Ultrasound, P. Miskine, Zagreb, Yugoslavia. For reprints contact Asim Kurjak, MD, PhD, Ultrasonic Institute, University of Zagreb, P. Miskine 64, 41000 Zagreb, Yugoslavia. 0 1990 by John Wiley & Sons, Inc.
CCC 0091-2751/90/040227-08 $04.00
is encoded as the amount of green and yellow mixed with red or blue, resulting in a mosaic appearance. The most important advantage of color Doppler is the display of blood flow over the whole scanning plane, as compared with only one line of sight available with conventional pulsed Doppler ultrasound techniques. Endosonography has also dramatically changed the profile of diagnostic ultrasonography. Esophageal, rectal, and vaginal probes provide superb visualization of the organs of interest. Optimal resolution is now being achieved, thus significantly increasing the sensitivity and specificity of ultrasound diagnosis. For this reason vaginal probes have been used extensively in the assessment of gynecological patients. The first reports have shown a significant improvement in the detection and characterization of adnexal masses (tumors, extrauterine pregnancy, etc.) when vaginal sonography has been compared with abdominal ultrasonography. Some reports have also shown the advantages attained by the former in the evaluation of first trimester pregnancy, as well as in the assessment of infertile patients.' Transvaginal sonography has been introduced 227
KURJAK ET AL.
228
into clinical practice simultaneously with the clinician’s growing awareness of the diagnostic value of blood studies by Doppler ultrasonography. Therefore, the introduction of vaginal Doppler studies has almost coincided with the first reports on vaginal sonography. The purpose of this study was to evaluate the potential contribution of color Doppler to ultrasound diagnosis by transvaginal imaging. PATIENTS AND METHODS
The value of color flow mapping has been studied in a group of 64 patients including 15 infertile patients undergoing ultrasound monitoring of folicular growth and ovulation, 18 gynecological patients scheduled for surgery because of varying clinically proven pelvic pathology, 2 patients with suspected ectopic pregnancy, and 29 patients in the 6th week to 10th week of unwanted pregnancy. All the patients were examined by an Aloka Color Doppler SSD-350 ultrasound scanner with color and pulsed Doppler capabilities. Examinations were performed using a 5-MHz real-time transvaginal probe, and included visualization of pelvic vessels and analysis of blood flow by color and pulsed Doppler. After the visualization of blood flow by color flow mapping, a pulsed Doppler beam was placed over the vessel of interest and blood flow velocity waveforms were recorded. Velocity waveforms analysis was performed by calculating the Resistance Index (RI).9 RESULTS
The external iliac arteries were seen by angulating the probe toward the lateral pelvic wall. Flow was successfully imaged in 108 out of 128 attempts (84.3%;left and right artery in each patient; Figure l ) . A similar result was obtained by analyzing flow in the internal iliac arteries. In most cases these vessels were visualized as passing posteriorly to the ovaries and flow was successfully imaged in 104 attempts (81.2%). The best results were achieved when flow in the uterine arteries was analyzed. Color Doppler clearly showed flow in all the examined cases (loo%),although the vessel itself could not be accurately defined on B-mode scan. The signals were easily obtained by running scans lateral to the uterine cervix. Further analysis included the examination of flow by pulsed Doppler ultrasonography. The placement of the Doppler beam was guided by color mapping, and the flow velocity waveforms obtained showed, in most cases,
characteristic signals with sustained diastolic flow (Figures 2 and 3). Unfortunately, analysis of flow in the ovarian arteries proved completely unsuccessful. Although the vessel-like structures were occasionaly visualized in B-scans on the posterolateral surface of the ovaries, blood flow could not be analyzed either by color Doppler or by pulsed Doppler ultrasonography (Table 1).The only feature of ovarian circulation that could be demonstrated was increased flow around the corpus luteum cyst. The vascularity of the corpus luteum was seen in 4 patients with proven ovulation in whom a cystic structure of the corpus luteum was reliably identified on B-scan in the luteal phase of the cycle (Figure 4). On pulsed Doppler examination it showed characteristics of low impedance flow with high diastolic velocities. In the subgroup of 18 patients with proven pelvic pathology, ultrasound examinations were performed preoperatively. In 10 cases a large uterine fibroma was found. Color Doppler showed blood flow within the tumor in 6 out of 10 cases, where it was regularly seen as flow in very thin vessels within the tumor (Figure 5), showing low velocity and low impedance waveform characteristics on pulsed Doppler evaluation. Moreover, in 4 of these 6 cases flow in the uterine artery showed a markedly lower impedance as compared with normal controls (Figure 6). In 6 cases the ovarian pathology was benign, and included 2 simple ovarian cysts, 2 endometriotic cysts, 1 dermoid cyst, and 1 chronic tubo-ovarian abscess. Meticulous examination revealed no flow within the tumor or in its surroundings in any of these cases. There were 2 cases of ovarian malignancy. In 1 case of primary ovarian malignancy the B-scan showed a complex solid cystic tumor in the right adnexal region. Color flow mapping revealed the presence of an extensive vascular supply within the solid part of the tumor. In the other case a retrouterine solid mass was detected in a patient who had been operated on 8 months earlier be-
TABLE 1 Visualization of Blood Flow in Major Pelvic Vessels by Color Doppler (N = 64) Left
Right External iliac artery Internal iliac artery Uterine artery Ovarian artery
N 58 54 64 0
(%)
(90.1) (79.7) (100) (0)
N 50 51 64 0
(70) (78.1) (73.4) (100) 10)
Total N 108 104 128 0
(%)
(84.31 (81.2) (100) 10)
JOURNAL OF CLINICAL ULTRASOUND
TRANSVAGINAL COLOR DOPPLER IMAGING
cause of adenocarcinoma of the ovary. In this case the presence of increased blood flow was also seen with color Doppler (Figure 7). In both cases pulsed Doppler examination showed high velocity and low impedance blood flow. Twenty-nine pregnant patients were examined in the first trimester of pregnancy (menstrual age: 6 to 10 weeks). In 27 patients ultrasound examination using the transvaginal probe revealed normal findings. In comparison with nonpregnant subjects, the color flow appearance of the uterine artery in this group was more pronounced owing to increased flow in diastole (Figure 8).This finding was confirmed by comparison of mean RI values obtained by flow velocity waveform analysis. The mean RI value in the nonpregnant subgroup was 0.84 2 0.07 and in pregnant cases 0.75 0.08, reflecting a slightly increased diastolic flow, although the observed difference was not statistically significant (t = 1 . 2 7 ;> ~ 0.05; N = 42). An interesting observation was the demonstration of blood flow in the trophoblast. Its visualization was gradually enhanced with advancing menstrual age up t o an overall success rate of 59% (16127; Table 2 and Figure 9). On pulsed Doppler examination it showed characteristics of low impedance flow with RI values significantly different from waveforms obtained from the uterine artery (t = 12.48; p < 0.01; n = 43; Figure 10). Blood flow in the fetal vessels, specifically the fetal aorta and umbilical arteries within the cord, was also assessed. Color flow mapping successfully demonstrated flow in the umbilical artery starting at 6 weeks and flow in the fetal aorta starting at 8 weeks (Table 2). The comon feature of the flow velocity waveforms in both of these vessels was the absence of diastolic flow in the pulsed Doppler evaluation. (Figures 11 and 12)
*
TABLE 2 Visualization of Blood Flow in the Fetal and Placental Vessels in the First Trimester of Pregnancy by Color Doppler (N = 27) ~~
Weeks
N
Trophoblast
6+
6 7 6
2 5 3
(33)
5
4
10'
3
TOTAL
27
N 7+ 8+ 9+
Umbilical Artery
Aorta
N
(%)
N
(Oh)
133)
0 0
(0) (0)
3
(50)
2
(80) (66)
2 7 6 5 3
16
(59)
23
VOL. 18. NO. 4, MAY 1990
(Oh)
(71) (50)
(100) (100)
(100)
4
(80)
(100)
3
(100)
(85)
10
(37)
229
There were also 2 cases of abnormal pregnancy. In 1 case of missed abortion diagnosed at 9 weeks, there was normal flow through the uterine artery but flow through the throphoblast was not demonstrated. The other case, a blighted ovum detected by ultrasound at 8 weeks of amenorrhea, proved more interesting. Color Doppler showed particularly pronounced flow in the trophoblast, which was unusually clear as compared with normal pregnancy. Pulsed Doppler analysis showed an RI value of 0.35, which was well below the mean value of 0.44 2 0.09 found in normal cases. Finally, there were 2 cases of tuba1 pregnancy diagnosed at 6 weeks and 7 weeks. In the first case the transvaginal B-scan showed a nonhomogeneous 3.8 cm mass in the right adnexal region. There were no signs of the embryo or gestational sac, and the color Doppler examination revealed nothing of particular interest. The mass later proved to be a hematocele. The second case involved a gestational sac-like structure between the uterus and the right ovary. The structure measured 1.2 cm in size, and there were no signs of embryo presence. Color flow mapping showed increased vascularity at the border of the sac. Pulsed Doppler examination guided by color mapping showed low impedance flow characteristics similar to trophoblast flow in normal early pregnancy. Laparotomy, performed a day later, confirmed the ultrasound finding (Figures 1315). DISCUSSION
The introduction of transvaginal sonography in gynecology has contributed significantly to the refinement and accuracy of ultrasound diagnosis in this field.4,5In addition to new morphological information that can be obtained by a high-frequency transvaginal probe, the combination of one probe and Doppler capability offers insights into dynamic studies of blood flow within the female pelvis. In comparison with previous experience in studies of blood flow in the female pelvis,lo-lz the results obtained by this technique have revealed some interesting new facts.8 In this study we examined the diagnostic information that can be obtained by color Doppler in the assessment of pelvic circulation. Blood flow was clearly seen in the internal and external iliac arteries in the majority of cases. This is not surprising considering the large diameter of these vessels and high blood flow velocity. However, from the clinical point of view, analysis of blood flow in the uterine and ovarian arteries is
230
KURJAK ET AL.
FIGURE 1. Doppler study of the external iliac artery (left). The characteristic flow vdocity waveform (right) was obtained by placing the sample volume of pulsed Doppler system over the vessel (right).
FIGURE 2. Blood flow (arrows) i n the uterine artery as seen by color flow mapping.
FIGURE 3. Characteristic flow velocity waveforms obtained by pulsed Doppler from a uterine artery previously visualized by color flow mapping (Figure 2).
FIGURE 4. Increased vascularity (arrow) in the corpus luteum as seen by color Doppler.
FIGURE 5. Preoperative scan of uterine fibroma demonstrating the presence of thin vessels within the tumor.
FIGURE 6. Increased flow through the uterine artery in a postmenopausal patient with uterine fibroma. JOURNAL OF CLINICAL ULTRASOUND
TRANSVAGINAL COLOR DOPPLER IMAGING
231
FIGURE 7. Demonstration of large vessels within a solid adnexal tumor in a case of recurrent ovarian malignancy.
FIGURE 8. Demonstration of blood flow in the uterine artery in early pregnancy (left). Flow velocity waveform showing reduced irnpedance in the vessel (right).
FIGURE 9. Vascularization of the trophoblast (arrow) as documented by color flow mapping in a normal 8-week-old pregnancy.
FIGURE 10. A low impedance flow velocity waveforms (right) that were obtained from the trophoblast.
FIGURE 11. Doppler signals obtained from the umbilical artery (arrow) showing no diastolic flow at 8 weeks.
FIGURE 14. Color flow mapping in the case as in Fig. 13 showing a highly vascularized area (arrows) within the wall of the sac.
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KURJAK ET AL.
FIGURE 12. Flow through the fetal aorta (left) and Doppler signals with no diastolic flow (right).
FIGURE 15. Pulsed Doppler signal from the vascular region seen in Figure 14 indicates the presence of low impedance flow, showing characteristics of flow in the troohoblast.
much more important. Experience with transabdominal studies has shown that the uterine arteries are very rarely seen in nonpregnant patients or in the first trimester of pregnancy, and signals are difficult to Our results have shown that color Doppler provides for easy and simple visualization of uterine arteries, and therefore for accurate and reproducible studies of blood flow within them. Unfortunately, the ovarian arteries, being particularly thin vessels, are hardly visualized by transvaginal scanning. Our attempts to visualize blood flow within them by color Doppler or to analyse flow patterns by pulsed Doppler were unsuccessful due to their position (relatively far from the transducer) and the presence of the bowel loops that surround the ovaries and prevent the penetration of Doppler signals. Clear and repro-
FIGURE 13. Gestational sac-like structure (arrows) demonstrated by transvaginal scan i n the right adnexal region.
ducible signals of these vessels can be obtained by sensitive transabdominal because the bowel loops are pushed outside the pelvis by a full urinary bladder, thus permitting easier penetration of Doppler signals. Our experience differs somewhat from the experience of other authors,' who claim that it is possible to obtain clear signals from ovarian arteries by transvaginal pulsed Doppler. However, they could not visualize the ovarian arteries either, and the signals were taken either from the surface of the ovaries or inside the ovarian parenchyma. A particularly interesting part of this study concerned the assessment of blood flow in pelvic tumors. It has been documented that any tumorous growth in the body has to be associated with the formation of new blood vessels. This process of neovascularization is much more pronounced in malignant tumors owing to the higher metabolism and rapid growth of tumorous tissue.13 These newly formed vessels are characterized by deficient development of muscular elements in the vessel wall, resulting in low flow resistance. Moreover, the numerous arteriovenous anastomoses that are usually present contribute t o high flow velocities due to high pressure gradients between the two vascular beds. This results in characteristic flow patterns that can be accurately assessed by Doppler ultrasound. The analysis of Doppler signals in the subgroup of patients who underwent surgery showed that the presence of newly formed vessels can be demonstrated both in benign and malignant conditions. More specifically, flow was visualized in 6 out of 10 benign myomas within the tumor tissue. However, the ability to demonstrate neovascularization within uterine fibromas is largely JOURNAL OF CLINICAL ULTRASOUND
TRANSVAGINAL COLOR DOPPLER IMAGING
dependent on the tumor size, and the position and extent of secondary degenerative changes. In the 2 cases of malignant ovarian tumors, newly formed vessels were seen in both. Comparison of flow characteristics between myomas and malignant ovarian tumors showed that the vessels observed in fibromatous tissue were typically very thin with low velocity flow. Conversely, in malignant tumors much wider vessels were relatively easy to identify, showing high velocity and low impedance flow characteristics. Histological type and growth rate of the tumor influences the process of neovascularization to a significant extent. Our results, although very preliminary, are in agreement with this hypothesis as well as with the results of other authors6 who have analyzed flow velocity patterns in abdominal tumors. If further clinical trials show that the analysis of blood flow characteristics can be used as a sufficiently reliable criterion for evaluation of tumor nature (benign vs. malignant type), the impact of ultrasound diagnosis in the management of patients with pelvic tumors would truly be a major one. The results obtained in the early pregnancy subgroup clearly showed that the analysis of blood flow in major embryonic vessels can be performed as early as the 6th week. Embryonic vessels can be easily visualized by color Doppler and the pulsed Doppler beam can thus be easily guided to the vessel of interest. The characteristics of blood flow in the aorta and umbilical artery were in agreement with other reported res u l t and ~ ~ ~ showed no diastolic flow during the first trimester. Color Doppler was found particularly useful in demonstrating trophoblastic flow. If only pulsed Doppler is used, the localization of blood flow in the trophoblast is a time-consuming and relatively difficult procedure. The guidance of a pulsed Doppler beam by color flow mapping helps locate those areas with the most abundant flow, and makes examination much faster and easier. The potential clinical applications of Doppler studies in the trophoblast and embryonic vessels have yet to be defined. At the moment, trophoblastic flow can be successfully used as an aid in ultrasound diagnosis of ectopic pregnancy. The limitations of ultrasound diagnosis of ectopic gestation before the 7th week when the fetal pole appears in the normally developing gestational sac are well known and extensively discussed.15Although the identification of the fetal pole and heart action outside the uterus permits an accurate diagnosis of ectopic pregnancy, VOL. 18,
NO. 4, MAY 1990
233
such findings are infrequently seen. In most cases ectopic pregnancy may be identified as a gestational sac outside the uterus without an embryonic pole. The morphological characteristics of the sac are usually not specific enough for a final diagnosis, but this finding, together with plasma p human chorionic gonadotropin values, is useful in reaching a final diagnosis. As illustrated by our case, the identification of trophoblastic flow in the sac wall allows for a final diagnosis based on the ultrasound finding alone. This should contribute significantly to the success of ultrasound diagnosis in this very common and serious clinical condition. In summary, the results of our study show that transvaginal color Doppler can be used successfully in the assessment of circulation in the female pelvis. The major advantage of color Doppler is the spatial display of blood flow, which provides for easy orientation concerning vascularity in certain scanning areas and facilitates a detailed analysis of flow velocity patterns by pulsed Doppler. This is particularly advantageous in the analysis of flow in thin vessels that are extremely difficult to identify by pulsed Doppler. In order to obtain signals from these vessels we have used a color Doppler device primarily designed for flow analysis in peripheral vessels, whereas most of presently available color Doppler devices are designed for blood flow studies in the heart and are not capable of clearly displaying flow in peripheral vessels. In spite of this, the major problem is still the inability to obtain signals from deeply situated thin vessels, such as ovarian arteries, owing to the low penetration of the Doppler beam. Our current experience has shown that ultrasound examination of pelvic circulation by a transvaginal probe combined with pulsed and color Doppler assessment may increase the reliability of ultrasound diagnosis in certain pathological pelvic conditions. The opportunity to analyze flow characteristics in pelvic vessels will undoubtedly provide new data on the physiology and pathophysiology of pelvic circulation, but further work is required before these data may be used in routine clinical work.
REFERENCES Switzer DF, Nanda NC: Doppler color flow mapping. Ultrasound Med Biol 11:403, 1985. Kurjak A, Breyer B, Jurkovic D, Alfirevic Z, Miljan M: Color flow mapping in obstetrics. J Perinat Med 15:271, 1987. Kurjak A, Alfirevic Z, Miljan M: Conventional
234
KURJAK ET AL.
and color Doppler in the assessment of fetal and maternal circulation. Ultrasound Med Biol 14:337, 1988. 4. Fleisher AC: Transvaginal sonography helps find ovarian cancer. Diagnost Zmag 10:124, 1988. 5. Trimor-Tritsch IE, Rottem S: Transvaginal Sonography. New York, Elsevier, 1987, p 36. 6. Taylor KJW: Doppler detects vascularity of some malignant tumors. Diagnost Zmag 10:132, 1988. 7. Kasai C, Namekawa K: Real-time two-dimensional blood flow imaging using ultrasound Doppler, in Recent Advances in Ultrasound Diagnosis (vol 51, Kurjak A, Kossoff G (eds). Amsterdam, Excerpta Medica, 1986, p 103. 8. McSweeney MB, Baber RJ, Gill RW, Kossoff G, Saunders D, Porter R, Piker R Prediction of IVF and gift outcome using transvaginal Doppler assessment of ovarian blood flow. J Ultrasound Med 7:S73, 1988. 9. Pourcelot L: Applications clinique de l’examen Doppler transcutane, in Velocimetrie ultrasonore Doppler (Vol. 34), Peronneau P (ed). Inserm, Paris, 1974, p 213. 10. Taylor KJW, Burns PN, Wells PNT, Conway DI,
Hull MGR: Ultrasound Doppler flow studies for the ovarian and uterine arteries. B r J Obstet Gynecol 92:240, 1985. 11. Kurjak A, Jurkovic D: New ultrasonic technique for assessing circulation in female pelvis, in Recent Advances in Ultrasound (Vol 5), Kurjak A, Kossoff G (eds). Excerpta Medica, Amsterdam, 1986, p 129. 12. Taylor KJW, Grannum PAT, DeCherney AH: Research lessons for maternal-fetal research from reproductive system studies, in Doppler Ultrasound Measurement of Maternal-Fetal Hemodynamics, Maulik D, McNellis D (eds). Perinatology Press, 1987, p 185. 13. Folkman J, Merler E, Abernathy C, Williams G: Isolation of a tumor factor responsible for angiogenesis. J Exp Med 33:275, 1971. 14. Griffiths K, Gill R, Torode H, Dixon K, O’Connell D: The umbilical artery in early pregnancy: When does diastolic flow appear? J Ultrasound Med 7(suppl):100, 1988. 15. Lawson TL: Ectopic pregnancy, criteria and accuracy of ultrasonic diagnosis. A J R 131:153, 1978.
JOURNAL OF CLINICAL ULTRASOUND
Transvaginal Color Doppler Imaging Asim Kurjak, MD, PhD, Davor Jurkovic, MD, Zarko Alfirevic, MD, and Ivica Zalud, MD
Abstract: Transvaginal color Doppler was used to assess circulation in pelvic vessels in a group of 64 patients including 15 patients with fertility problems, 18 patients with pelvic tumors, 2 cases of suspected ectopic pregnancy, and 29 pregnant patients with fetuses between 6 weeks and 10 weeks, menstrual age. Blood flow was successfully displayed by color Doppler in the external and internal iliac arteries, and the uterine atreries, but flow in ovarian arteries could not be visualized. In the subgroup of patients with pelvic tumors, neovascularization of tumor tissue was documented in 6 out of 10 cases of uterine fibroma and in 2 cases of ovarian cancer. In 6 cases involving benign ovarian pathology, no abnormal blood supply was observed. A comparison between the characteristics of blood flow within uterine fibromas and ovarian malignancies showed lower impedance and higher blood velocity in cases of malignancy. In early pregnancy blood flow in the umbilical artery could be visualized by color Doppler starting from the 6th week and flow in the aorta from the 8th week. Flow in the trophoblasts was observed with an overall success rate of 59% and successfully demonstrated in 1 out of 2 cases of ectopic pregnancy. Indexing Words: Doppler color imaging * Color imaging Transvaginal imaging
The most exciting recent developments in the field of diagnostic ultrasonography in obstetric and gynecology are, undoubtedly, color Doppler and transvaginal sonography.1-6 Color Doppler, or more precisely color-encoded real-time two-dimensional Doppler, imaging systems display flow as multiple points in a two-dimensional plane superimposed on a two-dimensional ultrasound image. The technique is based mainly on the moving target identification principle, which is, in fact, an autocorrelation techn i q ~ eA . ~delay line is used to bring data from subsequent images to a multiplier and the rate at which analogous signals are digitized in the scan converter provides continuous information on flow velocity. In the majority of commercially available units, flow toward the transducer is encoded in red, and flow going away from the transducer is encoded in blue. Flow velocity is proportional to the color brightness. Turbulence From the Ultrasonic Institute, University of Zagreb, WHO Collaborating Centre for Diagnostic Ultrasound, P. Miskine, Zagreb, Yugoslavia. For reprints contact Asim Kurjak, MD, PhD, Ultrasonic Institute, University of Zagreb, P. Miskine 64, 41000 Zagreb, Yugoslavia. 0 1990 by John Wiley & Sons, Inc.
CCC 0091-2751/90/040227-08 $04.00
is encoded as the amount of green and yellow mixed with red or blue, resulting in a mosaic appearance. The most important advantage of color Doppler is the display of blood flow over the whole scanning plane, as compared with only one line of sight available with conventional pulsed Doppler ultrasound techniques. Endosonography has also dramatically changed the profile of diagnostic ultrasonography. Esophageal, rectal, and vaginal probes provide superb visualization of the organs of interest. Optimal resolution is now being achieved, thus significantly increasing the sensitivity and specificity of ultrasound diagnosis. For this reason vaginal probes have been used extensively in the assessment of gynecological patients. The first reports have shown a significant improvement in the detection and characterization of adnexal masses (tumors, extrauterine pregnancy, etc.) when vaginal sonography has been compared with abdominal ultrasonography. Some reports have also shown the advantages attained by the former in the evaluation of first trimester pregnancy, as well as in the assessment of infertile patients.' Transvaginal sonography has been introduced 227
KURJAK ET AL.
228
into clinical practice simultaneously with the clinician’s growing awareness of the diagnostic value of blood studies by Doppler ultrasonography. Therefore, the introduction of vaginal Doppler studies has almost coincided with the first reports on vaginal sonography. The purpose of this study was to evaluate the potential contribution of color Doppler to ultrasound diagnosis by transvaginal imaging. PATIENTS AND METHODS
The value of color flow mapping has been studied in a group of 64 patients including 15 infertile patients undergoing ultrasound monitoring of folicular growth and ovulation, 18 gynecological patients scheduled for surgery because of varying clinically proven pelvic pathology, 2 patients with suspected ectopic pregnancy, and 29 patients in the 6th week to 10th week of unwanted pregnancy. All the patients were examined by an Aloka Color Doppler SSD-350 ultrasound scanner with color and pulsed Doppler capabilities. Examinations were performed using a 5-MHz real-time transvaginal probe, and included visualization of pelvic vessels and analysis of blood flow by color and pulsed Doppler. After the visualization of blood flow by color flow mapping, a pulsed Doppler beam was placed over the vessel of interest and blood flow velocity waveforms were recorded. Velocity waveforms analysis was performed by calculating the Resistance Index (RI).9 RESULTS
The external iliac arteries were seen by angulating the probe toward the lateral pelvic wall. Flow was successfully imaged in 108 out of 128 attempts (84.3%;left and right artery in each patient; Figure l ) . A similar result was obtained by analyzing flow in the internal iliac arteries. In most cases these vessels were visualized as passing posteriorly to the ovaries and flow was successfully imaged in 104 attempts (81.2%). The best results were achieved when flow in the uterine arteries was analyzed. Color Doppler clearly showed flow in all the examined cases (loo%),although the vessel itself could not be accurately defined on B-mode scan. The signals were easily obtained by running scans lateral to the uterine cervix. Further analysis included the examination of flow by pulsed Doppler ultrasonography. The placement of the Doppler beam was guided by color mapping, and the flow velocity waveforms obtained showed, in most cases,
characteristic signals with sustained diastolic flow (Figures 2 and 3). Unfortunately, analysis of flow in the ovarian arteries proved completely unsuccessful. Although the vessel-like structures were occasionaly visualized in B-scans on the posterolateral surface of the ovaries, blood flow could not be analyzed either by color Doppler or by pulsed Doppler ultrasonography (Table 1).The only feature of ovarian circulation that could be demonstrated was increased flow around the corpus luteum cyst. The vascularity of the corpus luteum was seen in 4 patients with proven ovulation in whom a cystic structure of the corpus luteum was reliably identified on B-scan in the luteal phase of the cycle (Figure 4). On pulsed Doppler examination it showed characteristics of low impedance flow with high diastolic velocities. In the subgroup of 18 patients with proven pelvic pathology, ultrasound examinations were performed preoperatively. In 10 cases a large uterine fibroma was found. Color Doppler showed blood flow within the tumor in 6 out of 10 cases, where it was regularly seen as flow in very thin vessels within the tumor (Figure 5), showing low velocity and low impedance waveform characteristics on pulsed Doppler evaluation. Moreover, in 4 of these 6 cases flow in the uterine artery showed a markedly lower impedance as compared with normal controls (Figure 6). In 6 cases the ovarian pathology was benign, and included 2 simple ovarian cysts, 2 endometriotic cysts, 1 dermoid cyst, and 1 chronic tubo-ovarian abscess. Meticulous examination revealed no flow within the tumor or in its surroundings in any of these cases. There were 2 cases of ovarian malignancy. In 1 case of primary ovarian malignancy the B-scan showed a complex solid cystic tumor in the right adnexal region. Color flow mapping revealed the presence of an extensive vascular supply within the solid part of the tumor. In the other case a retrouterine solid mass was detected in a patient who had been operated on 8 months earlier be-
TABLE 1 Visualization of Blood Flow in Major Pelvic Vessels by Color Doppler (N = 64) Left
Right External iliac artery Internal iliac artery Uterine artery Ovarian artery
N 58 54 64 0
(%)
(90.1) (79.7) (100) (0)
N 50 51 64 0
(70) (78.1) (73.4) (100) 10)
Total N 108 104 128 0
(%)
(84.31 (81.2) (100) 10)
JOURNAL OF CLINICAL ULTRASOUND
TRANSVAGINAL COLOR DOPPLER IMAGING
cause of adenocarcinoma of the ovary. In this case the presence of increased blood flow was also seen with color Doppler (Figure 7). In both cases pulsed Doppler examination showed high velocity and low impedance blood flow. Twenty-nine pregnant patients were examined in the first trimester of pregnancy (menstrual age: 6 to 10 weeks). In 27 patients ultrasound examination using the transvaginal probe revealed normal findings. In comparison with nonpregnant subjects, the color flow appearance of the uterine artery in this group was more pronounced owing to increased flow in diastole (Figure 8).This finding was confirmed by comparison of mean RI values obtained by flow velocity waveform analysis. The mean RI value in the nonpregnant subgroup was 0.84 2 0.07 and in pregnant cases 0.75 0.08, reflecting a slightly increased diastolic flow, although the observed difference was not statistically significant (t = 1 . 2 7 ;> ~ 0.05; N = 42). An interesting observation was the demonstration of blood flow in the trophoblast. Its visualization was gradually enhanced with advancing menstrual age up t o an overall success rate of 59% (16127; Table 2 and Figure 9). On pulsed Doppler examination it showed characteristics of low impedance flow with RI values significantly different from waveforms obtained from the uterine artery (t = 12.48; p < 0.01; n = 43; Figure 10). Blood flow in the fetal vessels, specifically the fetal aorta and umbilical arteries within the cord, was also assessed. Color flow mapping successfully demonstrated flow in the umbilical artery starting at 6 weeks and flow in the fetal aorta starting at 8 weeks (Table 2). The comon feature of the flow velocity waveforms in both of these vessels was the absence of diastolic flow in the pulsed Doppler evaluation. (Figures 11 and 12)
*
TABLE 2 Visualization of Blood Flow in the Fetal and Placental Vessels in the First Trimester of Pregnancy by Color Doppler (N = 27) ~~
Weeks
N
Trophoblast
6+
6 7 6
2 5 3
(33)
5
4
10'
3
TOTAL
27
N 7+ 8+ 9+
Umbilical Artery
Aorta
N
(%)
N
(Oh)
133)
0 0
(0) (0)
3
(50)
2
(80) (66)
2 7 6 5 3
16
(59)
23
VOL. 18. NO. 4, MAY 1990
(Oh)
(71) (50)
(100) (100)
(100)
4
(80)
(100)
3
(100)
(85)
10
(37)
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There were also 2 cases of abnormal pregnancy. In 1 case of missed abortion diagnosed at 9 weeks, there was normal flow through the uterine artery but flow through the throphoblast was not demonstrated. The other case, a blighted ovum detected by ultrasound at 8 weeks of amenorrhea, proved more interesting. Color Doppler showed particularly pronounced flow in the trophoblast, which was unusually clear as compared with normal pregnancy. Pulsed Doppler analysis showed an RI value of 0.35, which was well below the mean value of 0.44 2 0.09 found in normal cases. Finally, there were 2 cases of tuba1 pregnancy diagnosed at 6 weeks and 7 weeks. In the first case the transvaginal B-scan showed a nonhomogeneous 3.8 cm mass in the right adnexal region. There were no signs of the embryo or gestational sac, and the color Doppler examination revealed nothing of particular interest. The mass later proved to be a hematocele. The second case involved a gestational sac-like structure between the uterus and the right ovary. The structure measured 1.2 cm in size, and there were no signs of embryo presence. Color flow mapping showed increased vascularity at the border of the sac. Pulsed Doppler examination guided by color mapping showed low impedance flow characteristics similar to trophoblast flow in normal early pregnancy. Laparotomy, performed a day later, confirmed the ultrasound finding (Figures 1315). DISCUSSION
The introduction of transvaginal sonography in gynecology has contributed significantly to the refinement and accuracy of ultrasound diagnosis in this field.4,5In addition to new morphological information that can be obtained by a high-frequency transvaginal probe, the combination of one probe and Doppler capability offers insights into dynamic studies of blood flow within the female pelvis. In comparison with previous experience in studies of blood flow in the female pelvis,lo-lz the results obtained by this technique have revealed some interesting new facts.8 In this study we examined the diagnostic information that can be obtained by color Doppler in the assessment of pelvic circulation. Blood flow was clearly seen in the internal and external iliac arteries in the majority of cases. This is not surprising considering the large diameter of these vessels and high blood flow velocity. However, from the clinical point of view, analysis of blood flow in the uterine and ovarian arteries is
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FIGURE 1. Doppler study of the external iliac artery (left). The characteristic flow vdocity waveform (right) was obtained by placing the sample volume of pulsed Doppler system over the vessel (right).
FIGURE 2. Blood flow (arrows) i n the uterine artery as seen by color flow mapping.
FIGURE 3. Characteristic flow velocity waveforms obtained by pulsed Doppler from a uterine artery previously visualized by color flow mapping (Figure 2).
FIGURE 4. Increased vascularity (arrow) in the corpus luteum as seen by color Doppler.
FIGURE 5. Preoperative scan of uterine fibroma demonstrating the presence of thin vessels within the tumor.
FIGURE 6. Increased flow through the uterine artery in a postmenopausal patient with uterine fibroma. JOURNAL OF CLINICAL ULTRASOUND
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FIGURE 7. Demonstration of large vessels within a solid adnexal tumor in a case of recurrent ovarian malignancy.
FIGURE 8. Demonstration of blood flow in the uterine artery in early pregnancy (left). Flow velocity waveform showing reduced irnpedance in the vessel (right).
FIGURE 9. Vascularization of the trophoblast (arrow) as documented by color flow mapping in a normal 8-week-old pregnancy.
FIGURE 10. A low impedance flow velocity waveforms (right) that were obtained from the trophoblast.
FIGURE 11. Doppler signals obtained from the umbilical artery (arrow) showing no diastolic flow at 8 weeks.
FIGURE 14. Color flow mapping in the case as in Fig. 13 showing a highly vascularized area (arrows) within the wall of the sac.
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FIGURE 12. Flow through the fetal aorta (left) and Doppler signals with no diastolic flow (right).
FIGURE 15. Pulsed Doppler signal from the vascular region seen in Figure 14 indicates the presence of low impedance flow, showing characteristics of flow in the troohoblast.
much more important. Experience with transabdominal studies has shown that the uterine arteries are very rarely seen in nonpregnant patients or in the first trimester of pregnancy, and signals are difficult to Our results have shown that color Doppler provides for easy and simple visualization of uterine arteries, and therefore for accurate and reproducible studies of blood flow within them. Unfortunately, the ovarian arteries, being particularly thin vessels, are hardly visualized by transvaginal scanning. Our attempts to visualize blood flow within them by color Doppler or to analyse flow patterns by pulsed Doppler were unsuccessful due to their position (relatively far from the transducer) and the presence of the bowel loops that surround the ovaries and prevent the penetration of Doppler signals. Clear and repro-
FIGURE 13. Gestational sac-like structure (arrows) demonstrated by transvaginal scan i n the right adnexal region.
ducible signals of these vessels can be obtained by sensitive transabdominal because the bowel loops are pushed outside the pelvis by a full urinary bladder, thus permitting easier penetration of Doppler signals. Our experience differs somewhat from the experience of other authors,' who claim that it is possible to obtain clear signals from ovarian arteries by transvaginal pulsed Doppler. However, they could not visualize the ovarian arteries either, and the signals were taken either from the surface of the ovaries or inside the ovarian parenchyma. A particularly interesting part of this study concerned the assessment of blood flow in pelvic tumors. It has been documented that any tumorous growth in the body has to be associated with the formation of new blood vessels. This process of neovascularization is much more pronounced in malignant tumors owing to the higher metabolism and rapid growth of tumorous tissue.13 These newly formed vessels are characterized by deficient development of muscular elements in the vessel wall, resulting in low flow resistance. Moreover, the numerous arteriovenous anastomoses that are usually present contribute t o high flow velocities due to high pressure gradients between the two vascular beds. This results in characteristic flow patterns that can be accurately assessed by Doppler ultrasound. The analysis of Doppler signals in the subgroup of patients who underwent surgery showed that the presence of newly formed vessels can be demonstrated both in benign and malignant conditions. More specifically, flow was visualized in 6 out of 10 benign myomas within the tumor tissue. However, the ability to demonstrate neovascularization within uterine fibromas is largely JOURNAL OF CLINICAL ULTRASOUND
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dependent on the tumor size, and the position and extent of secondary degenerative changes. In the 2 cases of malignant ovarian tumors, newly formed vessels were seen in both. Comparison of flow characteristics between myomas and malignant ovarian tumors showed that the vessels observed in fibromatous tissue were typically very thin with low velocity flow. Conversely, in malignant tumors much wider vessels were relatively easy to identify, showing high velocity and low impedance flow characteristics. Histological type and growth rate of the tumor influences the process of neovascularization to a significant extent. Our results, although very preliminary, are in agreement with this hypothesis as well as with the results of other authors6 who have analyzed flow velocity patterns in abdominal tumors. If further clinical trials show that the analysis of blood flow characteristics can be used as a sufficiently reliable criterion for evaluation of tumor nature (benign vs. malignant type), the impact of ultrasound diagnosis in the management of patients with pelvic tumors would truly be a major one. The results obtained in the early pregnancy subgroup clearly showed that the analysis of blood flow in major embryonic vessels can be performed as early as the 6th week. Embryonic vessels can be easily visualized by color Doppler and the pulsed Doppler beam can thus be easily guided to the vessel of interest. The characteristics of blood flow in the aorta and umbilical artery were in agreement with other reported res u l t and ~ ~ ~ showed no diastolic flow during the first trimester. Color Doppler was found particularly useful in demonstrating trophoblastic flow. If only pulsed Doppler is used, the localization of blood flow in the trophoblast is a time-consuming and relatively difficult procedure. The guidance of a pulsed Doppler beam by color flow mapping helps locate those areas with the most abundant flow, and makes examination much faster and easier. The potential clinical applications of Doppler studies in the trophoblast and embryonic vessels have yet to be defined. At the moment, trophoblastic flow can be successfully used as an aid in ultrasound diagnosis of ectopic pregnancy. The limitations of ultrasound diagnosis of ectopic gestation before the 7th week when the fetal pole appears in the normally developing gestational sac are well known and extensively discussed.15Although the identification of the fetal pole and heart action outside the uterus permits an accurate diagnosis of ectopic pregnancy, VOL. 18,
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such findings are infrequently seen. In most cases ectopic pregnancy may be identified as a gestational sac outside the uterus without an embryonic pole. The morphological characteristics of the sac are usually not specific enough for a final diagnosis, but this finding, together with plasma p human chorionic gonadotropin values, is useful in reaching a final diagnosis. As illustrated by our case, the identification of trophoblastic flow in the sac wall allows for a final diagnosis based on the ultrasound finding alone. This should contribute significantly to the success of ultrasound diagnosis in this very common and serious clinical condition. In summary, the results of our study show that transvaginal color Doppler can be used successfully in the assessment of circulation in the female pelvis. The major advantage of color Doppler is the spatial display of blood flow, which provides for easy orientation concerning vascularity in certain scanning areas and facilitates a detailed analysis of flow velocity patterns by pulsed Doppler. This is particularly advantageous in the analysis of flow in thin vessels that are extremely difficult to identify by pulsed Doppler. In order to obtain signals from these vessels we have used a color Doppler device primarily designed for flow analysis in peripheral vessels, whereas most of presently available color Doppler devices are designed for blood flow studies in the heart and are not capable of clearly displaying flow in peripheral vessels. In spite of this, the major problem is still the inability to obtain signals from deeply situated thin vessels, such as ovarian arteries, owing to the low penetration of the Doppler beam. Our current experience has shown that ultrasound examination of pelvic circulation by a transvaginal probe combined with pulsed and color Doppler assessment may increase the reliability of ultrasound diagnosis in certain pathological pelvic conditions. The opportunity to analyze flow characteristics in pelvic vessels will undoubtedly provide new data on the physiology and pathophysiology of pelvic circulation, but further work is required before these data may be used in routine clinical work.
REFERENCES Switzer DF, Nanda NC: Doppler color flow mapping. Ultrasound Med Biol 11:403, 1985. Kurjak A, Breyer B, Jurkovic D, Alfirevic Z, Miljan M: Color flow mapping in obstetrics. J Perinat Med 15:271, 1987. Kurjak A, Alfirevic Z, Miljan M: Conventional
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and color Doppler in the assessment of fetal and maternal circulation. Ultrasound Med Biol 14:337, 1988. 4. Fleisher AC: Transvaginal sonography helps find ovarian cancer. Diagnost Zmag 10:124, 1988. 5. Trimor-Tritsch IE, Rottem S: Transvaginal Sonography. New York, Elsevier, 1987, p 36. 6. Taylor KJW: Doppler detects vascularity of some malignant tumors. Diagnost Zmag 10:132, 1988. 7. Kasai C, Namekawa K: Real-time two-dimensional blood flow imaging using ultrasound Doppler, in Recent Advances in Ultrasound Diagnosis (vol 51, Kurjak A, Kossoff G (eds). Amsterdam, Excerpta Medica, 1986, p 103. 8. McSweeney MB, Baber RJ, Gill RW, Kossoff G, Saunders D, Porter R, Piker R Prediction of IVF and gift outcome using transvaginal Doppler assessment of ovarian blood flow. J Ultrasound Med 7:S73, 1988. 9. Pourcelot L: Applications clinique de l’examen Doppler transcutane, in Velocimetrie ultrasonore Doppler (Vol. 34), Peronneau P (ed). Inserm, Paris, 1974, p 213. 10. Taylor KJW, Burns PN, Wells PNT, Conway DI,
Hull MGR: Ultrasound Doppler flow studies for the ovarian and uterine arteries. B r J Obstet Gynecol 92:240, 1985. 11. Kurjak A, Jurkovic D: New ultrasonic technique for assessing circulation in female pelvis, in Recent Advances in Ultrasound (Vol 5), Kurjak A, Kossoff G (eds). Excerpta Medica, Amsterdam, 1986, p 129. 12. Taylor KJW, Grannum PAT, DeCherney AH: Research lessons for maternal-fetal research from reproductive system studies, in Doppler Ultrasound Measurement of Maternal-Fetal Hemodynamics, Maulik D, McNellis D (eds). Perinatology Press, 1987, p 185. 13. Folkman J, Merler E, Abernathy C, Williams G: Isolation of a tumor factor responsible for angiogenesis. J Exp Med 33:275, 1971. 14. Griffiths K, Gill R, Torode H, Dixon K, O’Connell D: The umbilical artery in early pregnancy: When does diastolic flow appear? J Ultrasound Med 7(suppl):100, 1988. 15. Lawson TL: Ectopic pregnancy, criteria and accuracy of ultrasonic diagnosis. A J R 131:153, 1978.
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