Early
Human
Development,
29 (1992)
385
385-389
Elsevier Scientific Publishers Ireland Ltd. EHD 01308
Transvaginal color doppler assessmentof uteroplacental circulation in normal and abnormal early pregnancy A. Kurjaka, S. Kupesic-Urek”, M. Predanic”, A. Salihagicb “VItrasonic
Institute. University bPhysiology Institute,
of Zagreb, University
‘Sveti Duh’ Hospital, 64 Sveti Dub, 41ooO of Zagreb; 3 Salata, 41ooO Zagreb (Croatia)
Zagreb
and
Summary
Transvaginal color Doppler offers the potential to study uteroplacental circulation in early normal pregnancies and pregnancies associated with intrautine fibroids. A total of 62 patients (30 early pregnancies complicated by myoma and 32 normal pregnancies representing the control group) whose gestational age ranged from the 6th to the 14th week were examined. The equipment used was an Aloka color Doppler SSD-680 with 5.0 MHz curve-linear transvaginal transducer. The main uterine, radial and spiral arteries were identified in all patients. Peak systolic velocity and resistance index were measured and automatically calculated. Statistical analysis used was Student t-test. This study documents a physiological decrease in impedance in the uteroplacental circulation in pregnancy associated with fibroids, while the blood velocity of the radial arteries showed a significant increase between the 10th and 14th week of gestation. Key words: transvaginal color Doppler; uteroplacental circulation; early pregnancy; intrauterine fibroids
Introduction
The introduction of transvaginal color Doppler has allowed direct visualization of blood flow which is displayed simultaneously with the conventional B-mode image. Furthermore, color Doppler allows detection of blood flow in small vascular branches and increases the reproducibility of the measurements. The aim of this Correspondence to: A. Kujak, Duh, 41000 Zagreb, Croatia.
Ultrasonic Institute, University of Zagreb, ‘Sveti Dub’ Hospital, 64 Sveti
0378-3782/92/$05.00 0 1992 Elsevier Scientific Publishers Ireland Ltd. Printed and Published in Ireland
386
study was to use color Doppler to define blood flow characteristics of the uterine artery and it’s intrauterine branches (radial and spiral arteries) and to investigate blood flow changes in the uteroplacental circulation in early normal pregnancies and pregnancies associated with intrauterine fibroids. Patients and Methods A cross-sectional transvaginal color Doppler study of the uteroplacental circulation was performed on 62 patients. The mean age of the patients was 31 years (range 22-40 years). All the patients were divided into two groups: the first, early pregnancy complicated by myoma consisted of 30 women whose gestational age ranged from 6th to 14th weeks and the second of 32 women who represented control group. All the patients were examined by transvaginal color Doppler just before termination of pregnancy for psychosocial reasons. Clinically their pregnancies were considered normal, but ultrasonical examination demonstrated abnormal uterine morphology in first group, while in second group of patients uterine and adnexal morphology were normal. The equipment used in this study was Aloka color Doppler SSD 680 with 5.0 MHz curve-linear transvaginal transducer (Aloka Color Co, Tokyo, Japan). Pulsed repetition frequencies ranged from 2-23 kHz, depending on blood velocities in the vessel under investigation. The high pass filter was set on 100 Hz to eliminate lowfrequency signals occurring from pulsation of vessel walls. The spatial peak temporal average (SPTA) was approximately 80 mW cme2. Color Doppler examinations were performed by the same observer. The patients were lying in a supine position on the examination table with their knees bent. The transvaginal probe was gently introduced into the posterior fornix of the vagina after voiding of the patients. Morphology of the uterus and ovaries were explored by B-mode sonography. Color Doppler was used to visualize the blood flow of the uterine artery and it’s intrauterine branches: radial and spiral arteries in the control group; and arteries which surround and supply myomas (radial arteries) as well as spiral arteries in a group of complicated pregnancies. When color flow was seen pulsed Doppler signals were obtained using a 2-mm volume cursor. Blood flow impedance was reflected as resistance index (RI = (systole - dyastole)/systole), used as the calculation measurement of the blood flow velocity waveforms. The average blood velocity was calculated automatically from frequency of the ultrasound beam emitted from the transducer, as well as the mean Doppler shift, the speed of the ultrasound in tissue and the angle of approach between the ultrasound beam and the axis of the blood vessels. A recording was considered satisfactory for measurements when there were at list five equally intense waveforms in a row. The average duration of procedure was 20 min. The main uterine artery was visualized at the level of the internal OS as it approaches the uterus laterally and curves upward alongside the uterine body. Radial arteries were identified at their characteristic anatomical position within the myometrium. In the cases of the myomas, these arteries were used to study fibroids vascularity. The term ‘spiral arteries’ was used to determine the highly vascular area which was
387 RI
RI
RI
6 a
10
12
14 GA
6 a
10
12
6 a 10 12
14
GA
14 GA
Fig. 1. Comparison between mean values of resistance index (RI) in the uteroplacental circulation of normal pregnancies and pregnancies associated with uterine fibroids: ---, normal pregnancy; -, pregnancy associated with uterine fibroids; GA, gestational age (weeks).
visualized by color Doppler immediately below the placenta. Statistical analysis used was Student t-test.
The main uterine, radial and spiral arteries were clearly identified in all the cases with their characteristic waveform profile - low in the main uterine artery and moderate to high end diastolic velocity in radial and spiral artery. The difference between these arteries were in the value of RI and the velocity of the blood stream. Radial arteries were characterized with moderate to high end-diastolic velocities and resistance index lower than obtainable in the main uterine artery. Spiral arteries demonstrated with color Doppler in all examined patients, had low resistance index, but the maximum flow velocity didn’t differ from acquired radial artery waveforms. Significant changes for the peak systolic velocity and resistance index in uterine, radial and spiral arteries in correlation to gestational age were noticed in both examined groups (Figs 1 and 2). There were significant changes with gestation for peak systolic velocity and resistance index in the uterine arteries in both groups (P < O.OOl), without significant differences between groups (P > 0.01). The mean values for the peak systolic velocities and resistance index of radial arteries were significantly lower than the corresponding ones for the uterine artery
PSV
PSV (cm/s) 150 120 4
(cm/s)
1501
90
60 30 0
PSV 150 120 90 60
(cm/s)
.___---
,,;-;
14 6 8 10 12 14 6 a lo 12 14 GA GA GA Fig. 2. Comparison between mean values of peak systolic velocity (PSV) in the uteroplacental circulation of normal pregnancies and pregnancies associated with uterine fibroids. The asterisk denotes significant difference between mean values, but only from the 10th to the 14th week of the gestational age (GA); --- , normai pregnancy; -, pregnancy associated with uterine fibroids. 6 8, 10
12
388 PSV
(cm/s)
3
4
5
6
7cm
3
4
5
6
7cm
Fig. 3. Mean values of peak systolic velocity (PSV) and resistance index (RI) measured in radial arteries, with mean diameter (D) of uterine fibroids.
(P < 0.001). Signiticant difference between mean values for the peak systolic velocity was noticed only between 10th and 14th week of gestational age (P < 0.01) (Fig. 2).
Similarly, in the spiral artery, the mean values of the resistance index were significantly lower than the corresponding ones for the radial arteries (P < 0.001). However, there were no significant differences in the mean resistance index and peak systolic velocity between the groups (P > 0.01). A downward trend for the peak systolic velocity and resistance index in correlation with mean diameter of the observed myoma is noticed (Fig 3). Discussion Superb quality of the endovaginal B-mode image, superimposed on color Doppler, allows visualization of the uterine arteries and its branches: radial and spiral arteries, in early pregnancy. Characteristic flow velocity waveforms were found. Differences between these velocity waveforms are determined by vascular impedance and the velocity of the blood stream. Visualization of these arteries was possible in all cases. Although significant difference in blood velocity and RI values of the uterine arteries between nonpregnant women with and without uterine myomas exist [l-3], it would be assumable to find similar findings between the group of pregnant women with normal uterus anatomy and pregnancy complicated with myoma. Furthermore, it would be acceptable to obtain significant difference in RI value of blood flow in uterine arteries and its branches, especially radial arteries. Jurkovic at al. [4] reported significant increase of blood flow velocity in main uterine, radial and spiral arteries, as well as decreasing of RI values, corresponding to the gestational age of normal pregnant women. We obtained similar results as reported, but with no difference between examined groups. Combining these assumptions and reported values in comparison with our results, it is possible to speculate why our findings failed to show increased blood flow in the group where pregnancy was associated with fibroids. The increased blood flow of uterine vessel network (especially main arteries), due to hormonal placental and luteal body activity, ‘hide’ the subtle amount of increased blood flow caused by myoma metabolism. Radial artery blood flow analysis showed significant difference from the 10th to the 14th week of gestation. We believe, that increased blood flow in radial arteries which supply myoma is caused by higher levels of estriol hormone who is metabolized in placenta [5]. This hormone directly influences the increased metabolism of myoma cells, also causing
389
increased blood velocity in these arteries. All these changes in vascular perfusion of uterine vessels have not influenced the increased blood flow in spiral arteries. The RI values and blood flow velocity were the same in both groups and these values were higher with aging of gestation. Increased metabolism of myoma cells also determines increased blood velocity in these arteries. All these changes on uterine vascular perfusion in a group of patient with myomas have not influenced the increased blood flow in spiral arteries. The RI values and blood flow velocity were the same in both groups and these values were higher with gestational aging. The vessels observed on the periphery of the benign uterine tumors were thin with low velocity flow. The decrease of blood flow in arteries supplying myoma could be explained by the increase of the myoma’s with consequently higher peripheral impedance. The diastolic flow was increased in comparison with uterine artery blood flow, with RI moderately high to very high. Lower values of the RI in these arteries in comparison with the size of myoma are probably consequences of increased hormonal levels during the pregnancy. In conclusion, transvaginal color Doppler allows examination of the small arteries of uterus vascular network, which was impossible to demonstrate by previous conventional Doppler techniques, especially in early pregnancy. This study has documented a physiological decrease in impedance (RI) in the uteroplacental circulation in pregnancy associated with fibroids, while the blood velocity of the radial arteries showed significant higher increase between the 10th and the 14th week of gestational age. Myomas in pregnancy do not show any pathophysiological changes in uteroplacental circulation in the first trimester of pregnancy, that may predict the development of some complications such as preeclampsia or intrauterine growth retardation. Further investigations are required to examine the quality of blood flow in second and third trimesters in order to seek for other information of possible changes in blood perfusion of the uterus in pregnancies associated with fibroids. References 1 Kurjak, A. and Zalud, I. (1991): Uterine masses.In: Transvaginal Color Doppler, pp. l23- 135. Parthenon Publishing, Lancashire, UK, 2 Kurjak, A., Zalud, I., Jurkovic, D., Allirevic, Z. and Miljan, M. (1989): Transvaginal color Doppler in the assessment of pelvic circulation. Acta Obstet. Gynecol. &and., 68, 131. 3 Hata, T., Hata, K., Senoh, D., Manihara, K., Aoki, S., Takamija, 0. and Kitao, M. (1989): Doppler ultrasound assessment of tumor vascularisaty in gynecological dissorders. J. Ultrasound Med., 8, 1309. 4 Jurkovic, D., Jauniaux, E., Kurjak, A., Hustin, J., Campbell, S. and Nicolaides, K. (1991): Transvaginal color Doppler assessment of uteroplacental circulation in early pregnancy. Obstet. Gynecol., 77, 365. 5 Brasens, I., Robertonn, W.B. and Drekons, H.G. (1967): The physiological respons of the vessels at the placental bed to normal pregnancy. J. Pathol. Bact., 93, 569.
Human
Development,
29 (1992)
385
385-389
Elsevier Scientific Publishers Ireland Ltd. EHD 01308
Transvaginal color doppler assessmentof uteroplacental circulation in normal and abnormal early pregnancy A. Kurjaka, S. Kupesic-Urek”, M. Predanic”, A. Salihagicb “VItrasonic
Institute. University bPhysiology Institute,
of Zagreb, University
‘Sveti Duh’ Hospital, 64 Sveti Dub, 41ooO of Zagreb; 3 Salata, 41ooO Zagreb (Croatia)
Zagreb
and
Summary
Transvaginal color Doppler offers the potential to study uteroplacental circulation in early normal pregnancies and pregnancies associated with intrautine fibroids. A total of 62 patients (30 early pregnancies complicated by myoma and 32 normal pregnancies representing the control group) whose gestational age ranged from the 6th to the 14th week were examined. The equipment used was an Aloka color Doppler SSD-680 with 5.0 MHz curve-linear transvaginal transducer. The main uterine, radial and spiral arteries were identified in all patients. Peak systolic velocity and resistance index were measured and automatically calculated. Statistical analysis used was Student t-test. This study documents a physiological decrease in impedance in the uteroplacental circulation in pregnancy associated with fibroids, while the blood velocity of the radial arteries showed a significant increase between the 10th and 14th week of gestation. Key words: transvaginal color Doppler; uteroplacental circulation; early pregnancy; intrauterine fibroids
Introduction
The introduction of transvaginal color Doppler has allowed direct visualization of blood flow which is displayed simultaneously with the conventional B-mode image. Furthermore, color Doppler allows detection of blood flow in small vascular branches and increases the reproducibility of the measurements. The aim of this Correspondence to: A. Kujak, Duh, 41000 Zagreb, Croatia.
Ultrasonic Institute, University of Zagreb, ‘Sveti Dub’ Hospital, 64 Sveti
0378-3782/92/$05.00 0 1992 Elsevier Scientific Publishers Ireland Ltd. Printed and Published in Ireland
386
study was to use color Doppler to define blood flow characteristics of the uterine artery and it’s intrauterine branches (radial and spiral arteries) and to investigate blood flow changes in the uteroplacental circulation in early normal pregnancies and pregnancies associated with intrauterine fibroids. Patients and Methods A cross-sectional transvaginal color Doppler study of the uteroplacental circulation was performed on 62 patients. The mean age of the patients was 31 years (range 22-40 years). All the patients were divided into two groups: the first, early pregnancy complicated by myoma consisted of 30 women whose gestational age ranged from 6th to 14th weeks and the second of 32 women who represented control group. All the patients were examined by transvaginal color Doppler just before termination of pregnancy for psychosocial reasons. Clinically their pregnancies were considered normal, but ultrasonical examination demonstrated abnormal uterine morphology in first group, while in second group of patients uterine and adnexal morphology were normal. The equipment used in this study was Aloka color Doppler SSD 680 with 5.0 MHz curve-linear transvaginal transducer (Aloka Color Co, Tokyo, Japan). Pulsed repetition frequencies ranged from 2-23 kHz, depending on blood velocities in the vessel under investigation. The high pass filter was set on 100 Hz to eliminate lowfrequency signals occurring from pulsation of vessel walls. The spatial peak temporal average (SPTA) was approximately 80 mW cme2. Color Doppler examinations were performed by the same observer. The patients were lying in a supine position on the examination table with their knees bent. The transvaginal probe was gently introduced into the posterior fornix of the vagina after voiding of the patients. Morphology of the uterus and ovaries were explored by B-mode sonography. Color Doppler was used to visualize the blood flow of the uterine artery and it’s intrauterine branches: radial and spiral arteries in the control group; and arteries which surround and supply myomas (radial arteries) as well as spiral arteries in a group of complicated pregnancies. When color flow was seen pulsed Doppler signals were obtained using a 2-mm volume cursor. Blood flow impedance was reflected as resistance index (RI = (systole - dyastole)/systole), used as the calculation measurement of the blood flow velocity waveforms. The average blood velocity was calculated automatically from frequency of the ultrasound beam emitted from the transducer, as well as the mean Doppler shift, the speed of the ultrasound in tissue and the angle of approach between the ultrasound beam and the axis of the blood vessels. A recording was considered satisfactory for measurements when there were at list five equally intense waveforms in a row. The average duration of procedure was 20 min. The main uterine artery was visualized at the level of the internal OS as it approaches the uterus laterally and curves upward alongside the uterine body. Radial arteries were identified at their characteristic anatomical position within the myometrium. In the cases of the myomas, these arteries were used to study fibroids vascularity. The term ‘spiral arteries’ was used to determine the highly vascular area which was
387 RI
RI
RI
6 a
10
12
14 GA
6 a
10
12
6 a 10 12
14
GA
14 GA
Fig. 1. Comparison between mean values of resistance index (RI) in the uteroplacental circulation of normal pregnancies and pregnancies associated with uterine fibroids: ---, normal pregnancy; -, pregnancy associated with uterine fibroids; GA, gestational age (weeks).
visualized by color Doppler immediately below the placenta. Statistical analysis used was Student t-test.
The main uterine, radial and spiral arteries were clearly identified in all the cases with their characteristic waveform profile - low in the main uterine artery and moderate to high end diastolic velocity in radial and spiral artery. The difference between these arteries were in the value of RI and the velocity of the blood stream. Radial arteries were characterized with moderate to high end-diastolic velocities and resistance index lower than obtainable in the main uterine artery. Spiral arteries demonstrated with color Doppler in all examined patients, had low resistance index, but the maximum flow velocity didn’t differ from acquired radial artery waveforms. Significant changes for the peak systolic velocity and resistance index in uterine, radial and spiral arteries in correlation to gestational age were noticed in both examined groups (Figs 1 and 2). There were significant changes with gestation for peak systolic velocity and resistance index in the uterine arteries in both groups (P < O.OOl), without significant differences between groups (P > 0.01). The mean values for the peak systolic velocities and resistance index of radial arteries were significantly lower than the corresponding ones for the uterine artery
PSV
PSV (cm/s) 150 120 4
(cm/s)
1501
90
60 30 0
PSV 150 120 90 60
(cm/s)
.___---
,,;-;
14 6 8 10 12 14 6 a lo 12 14 GA GA GA Fig. 2. Comparison between mean values of peak systolic velocity (PSV) in the uteroplacental circulation of normal pregnancies and pregnancies associated with uterine fibroids. The asterisk denotes significant difference between mean values, but only from the 10th to the 14th week of the gestational age (GA); --- , normai pregnancy; -, pregnancy associated with uterine fibroids. 6 8, 10
12
388 PSV
(cm/s)
3
4
5
6
7cm
3
4
5
6
7cm
Fig. 3. Mean values of peak systolic velocity (PSV) and resistance index (RI) measured in radial arteries, with mean diameter (D) of uterine fibroids.
(P < 0.001). Signiticant difference between mean values for the peak systolic velocity was noticed only between 10th and 14th week of gestational age (P < 0.01) (Fig. 2).
Similarly, in the spiral artery, the mean values of the resistance index were significantly lower than the corresponding ones for the radial arteries (P < 0.001). However, there were no significant differences in the mean resistance index and peak systolic velocity between the groups (P > 0.01). A downward trend for the peak systolic velocity and resistance index in correlation with mean diameter of the observed myoma is noticed (Fig 3). Discussion Superb quality of the endovaginal B-mode image, superimposed on color Doppler, allows visualization of the uterine arteries and its branches: radial and spiral arteries, in early pregnancy. Characteristic flow velocity waveforms were found. Differences between these velocity waveforms are determined by vascular impedance and the velocity of the blood stream. Visualization of these arteries was possible in all cases. Although significant difference in blood velocity and RI values of the uterine arteries between nonpregnant women with and without uterine myomas exist [l-3], it would be assumable to find similar findings between the group of pregnant women with normal uterus anatomy and pregnancy complicated with myoma. Furthermore, it would be acceptable to obtain significant difference in RI value of blood flow in uterine arteries and its branches, especially radial arteries. Jurkovic at al. [4] reported significant increase of blood flow velocity in main uterine, radial and spiral arteries, as well as decreasing of RI values, corresponding to the gestational age of normal pregnant women. We obtained similar results as reported, but with no difference between examined groups. Combining these assumptions and reported values in comparison with our results, it is possible to speculate why our findings failed to show increased blood flow in the group where pregnancy was associated with fibroids. The increased blood flow of uterine vessel network (especially main arteries), due to hormonal placental and luteal body activity, ‘hide’ the subtle amount of increased blood flow caused by myoma metabolism. Radial artery blood flow analysis showed significant difference from the 10th to the 14th week of gestation. We believe, that increased blood flow in radial arteries which supply myoma is caused by higher levels of estriol hormone who is metabolized in placenta [5]. This hormone directly influences the increased metabolism of myoma cells, also causing
389
increased blood velocity in these arteries. All these changes in vascular perfusion of uterine vessels have not influenced the increased blood flow in spiral arteries. The RI values and blood flow velocity were the same in both groups and these values were higher with aging of gestation. Increased metabolism of myoma cells also determines increased blood velocity in these arteries. All these changes on uterine vascular perfusion in a group of patient with myomas have not influenced the increased blood flow in spiral arteries. The RI values and blood flow velocity were the same in both groups and these values were higher with gestational aging. The vessels observed on the periphery of the benign uterine tumors were thin with low velocity flow. The decrease of blood flow in arteries supplying myoma could be explained by the increase of the myoma’s with consequently higher peripheral impedance. The diastolic flow was increased in comparison with uterine artery blood flow, with RI moderately high to very high. Lower values of the RI in these arteries in comparison with the size of myoma are probably consequences of increased hormonal levels during the pregnancy. In conclusion, transvaginal color Doppler allows examination of the small arteries of uterus vascular network, which was impossible to demonstrate by previous conventional Doppler techniques, especially in early pregnancy. This study has documented a physiological decrease in impedance (RI) in the uteroplacental circulation in pregnancy associated with fibroids, while the blood velocity of the radial arteries showed significant higher increase between the 10th and the 14th week of gestational age. Myomas in pregnancy do not show any pathophysiological changes in uteroplacental circulation in the first trimester of pregnancy, that may predict the development of some complications such as preeclampsia or intrauterine growth retardation. Further investigations are required to examine the quality of blood flow in second and third trimesters in order to seek for other information of possible changes in blood perfusion of the uterus in pregnancies associated with fibroids. References 1 Kurjak, A. and Zalud, I. (1991): Uterine masses.In: Transvaginal Color Doppler, pp. l23- 135. Parthenon Publishing, Lancashire, UK, 2 Kurjak, A., Zalud, I., Jurkovic, D., Allirevic, Z. and Miljan, M. (1989): Transvaginal color Doppler in the assessment of pelvic circulation. Acta Obstet. Gynecol. &and., 68, 131. 3 Hata, T., Hata, K., Senoh, D., Manihara, K., Aoki, S., Takamija, 0. and Kitao, M. (1989): Doppler ultrasound assessment of tumor vascularisaty in gynecological dissorders. J. Ultrasound Med., 8, 1309. 4 Jurkovic, D., Jauniaux, E., Kurjak, A., Hustin, J., Campbell, S. and Nicolaides, K. (1991): Transvaginal color Doppler assessment of uteroplacental circulation in early pregnancy. Obstet. Gynecol., 77, 365. 5 Brasens, I., Robertonn, W.B. and Drekons, H.G. (1967): The physiological respons of the vessels at the placental bed to normal pregnancy. J. Pathol. Bact., 93, 569.
