Color and pulsed Doppler examinations of uterine blood flow

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					                              THESES




       Prenatal and neonatal medicine accredited PhD program
       (Program director: Professor Papp Zoltán MD, PhD, D.Sc.)




Color and pulsed Doppler examinations of uterine blood flow in
             normal and complicated pregnancies




                     Written by: Szabó István MD
                            Senior lecturer
             Semmelweis University, Faculty of Medicine
             1st Department of Obstetrics and Gynecology




                           Budapest, 2002




                                                                  1
Introduction


       As a consequence of the spectacular changes over the past few decades,
sonography has become one of the most important diagnostic tools in obstetrics and
gynaecology. Nowadays, it is suitable not only for detailed morphological investigation,
but for the identification of blood flow characteristics, too. The introduction of
continuous wave (CW) Doppler (Fitzgerald and Drumm, 1977) was the first step
toward assessing circulatory changes in various blood vessels and making functional
conclusions. The joint application of color and pulsed Doppler imaging technologies,
which have been more and more widespread since the late 1980s, is one of the most
recent developments in sonography. Color Doppler imaging (CDI) depicts blood flow in
colors on the conventional two-dimensional image, therefore, it is more suitable for the
evaluation of blood flow in selected areas than any previous non-invasive method.
Blood flow investigations can be performed even in small blood vessels, which can not
be identified with traditional sonography.
       The joint application of color and duplex methods has opened new perspectives
for the in-vivo study of circulatory changes during pregnancy. Processes cause
significant changes in uterine perfusion and implantation considerably rearranges
maternal circulation. Regular uterine circulation adjusts first to the needs of the
developing embryo, then to those of the fetus to which it is capable of providing all
nutrition and respiration. Uterine blood flow is of fundamental significance for the
outcome of the pregnancy.
       Color Doppler imaging was first implemented in obstetric and gynaecologic
examinations in the 1st Department of Obstetrics and Gynecology, Semmelweis
University in 1991. The author began to study uterine blood flow in normal and
complicated pregnancies with CDI at that time. The experiences collected during these
investigations are summed up in the present Ph.D. thesis.




                                                                                      2
Objectives


   Based on a diagnostic method, which provides the possibility for the assessment of
uterine vascular network and the evaluation of blood flow characteristics of various
blood vessels during pregnancy, from conception to delivery, the following objectives
were established for our successive series of investigations:


1. How does early pregnancy affect uterine blood flow and how can the uterine
   vascular network be characterised?
2. What characteristic features of ectopic pregnancy can be detected with CDI? How
   does abnormal implantation affect uterine blood flow?
3. What are the characteristics of uterine artery blood flow in the second half of a
   normal pregnancy? How do RI and PI values, as well as normal reference ranges for
   velocity indices change? How do resistance indices and velocity characteristics
   relate?
4. How is uterine circulation affected in normal pregnancies after bilateral hypogastric
   artery ligature?
5. How do the PI values of the uterine artery change in various forms of hypertension
   in pregnancy and in normotensive pregnancies complicated by intrauterine growth
   retardation?
6. What blood flow characteristics can be detected in uterine arteries in pregnancies
   complicated with severe pre-eclampsia? Can characteristic differences be detected
   for comparison with normal pregnancies?




                                                                                      3
Method


        Patients at the 1st Department of Obstetrics and Gynecology, Semmelweis
University participated in the study, which was previously approved by the clinic’s Ethical
Committee. Patients included females who reported to our outpatient department for
complicated early pregnancy care (often by referral), routine gynecological examinations,
and desired non-indicated abortion in normal early pregnancies, routine low-risk prenatal
care, or high-risk/pathological pregnancy care (often by referral). All patients received full
information regarding the aim and conditions of the study before testing was commenced.
Investigations were performed only in-patients who consented to the examination after
being explicitly informed.
        The examination results of 651 patients who appeared on 857 occasions between
July 1991 and December 2000 were processed in this study. Statistical data of gravid
patients and non-gravid patients in the fertile age range are summed up in Table 1.


                                Number       Age range      Days since last     Gestational
                                of cases      (years)      menstrual period     age (weeks)


Non-gravid women in the
                                  104          17-41
fertile age range

Normal early pregnancy             53          17-39                                5-14
Ectopic pregnancy                  49          17-36             32-71
Normal pregnancy                  247          18-39                               19-40
Pregnancy with previous            1             21                                12-34
bilateral hypogastric artery
ligature

Chronic hypertension               11          23-35                               26-40
Intrauterine retardation in        38          18-41                               26-40
normotensive pregnancy
Pre-eclampsia                     148          15-44                               25-37


Table 1. Statistical data of gravid patients and non-gravid patients in the fertile age range



                                                                                                4
       Gestational age was calculated from the last menstrual period using Naegeles’ rule,
and confirmed by crown-rump length (CRL), and later biparietal diameter and femur length
measurements. Calculated gestational age was used if the date of the last menstrual period
was certain and if the dating by first trimester ultrasound was within a range of 7 days from
the calculated gestational age.
       To define the normal standards, we only included cases where the gestational age
was correct and no fetal abnormalities or chromosomal aberrations were found during the
pregnancy or after birth. Balanced intrauterine development was found during the repeated
ultrasound biometry, and birth weights were between the 10th and 90th percentiles. We only
researched healthy pregnancies without chronic diseases, without carbohydrate metabolism
problems during the gestation and among which we found no changes relating to
intrauterine infection in the embryo/fetus.
       All sonograms were performed by the same specialist (Dr. Szabó István) in the 1st
Department Obstetrics and Gynecology of Semmelweis University with an ATL Ultramark
9 (Advanced Technology Laboratories, Seattle, WA, USA) scanner which is suitable for
2D, color and pulse Doppler examinations. This equipment provides the opportunity to
calculate the resistance index (RI) and pulsatility index (PI), as well as to determine peak
systolic velocity (PSV) and mean velocity (MV) at the same time.
       A 5 MHz convex electronic vaginal transducer was used for transvaginal
examinations in gynecological patients and in early pregnancy until the 14th week of
gestation. The transvaginal transducer produced a 90° sector. Blood flow was displayed at
depths from 2 to 123 millimetres. Flow toward the transducer was colored red and flow
away from the transducer was colored blue. The degree of turbulence was estimated and
depicted as the amount of green mixed with red and blue. A 2-mm Doppler sample volume
was used and the wall filter was set at 100 Hz to eliminate a low frequency signal caused by
noise. Pulse repetition frequency ranged from 1,200-12,000 Hz and enabled the detection of
blood flow velocity between 0.1 and 150 cm/sec.
       A 3.5 MHz convex electronic abdominal transducer (76 mm curved array) was used
from the 15th. week of gestation on. The transabdominal probe produced a 60° sector in
which the blood flow could be displayed at depths from 10 to 215 millimetres. Pulse



                                                                                           5
repetition frequency ranged from 3,000-17,000 Hz, which enabled the detection of blood
flow velocity between 5 and 300 cm/sec. A 2-3 mm Doppler sample volume was used
during pulsed Doppler examinations and the high pass filter was also set at 100 Hz to
eliminate noise.
       Conventional real-time imaging was performed in each patient to identify normal or
abnormal morphology. Color Doppler flow imaging was carried out to identify the different
vessels. When an appropriate vessel was identified, on-line spectral Doppler analysis was
performed on definable measuring points, which are well known from the literature. In this
arterial waveform analysis the peak systolic and mean velocities were determined and the
resistance and pulsatility index calculated. During the examination of larger uterine vessels,
when the angle between the ultrasound beam and direction of blood flow was less than 60°
(average between 15°and 50°) approximately real velocities can be detected after angle
correction.
       Only sharp, clear-bordered Doppler spectrums were considered usable. After
registering 4 to 5 characteristic waves of similar quality and maximal intensity, a
subsequent angle correction was made and the characteristics of the blood flow were
determined by the Doppler frequency shift analysis. Resistance and pulsatility indices were
calculated and peak systolic and mean velocities were determined. The qualitative
characteristics of the waveforms were also investigated and registered.
       When the vessel's axis was indefinable in small tortuous vessels (corpus luteum,
radial and spiral arteries, peritrophoblastic flow), the sample point of the pulsed Doppler
beam was positioned on the most brightly colored region. Blood flow velocity waveforms
with maximum amplitude and frequency shift were recorded. For PSV measurements,
angle correction was not carried out, as it has been shown that this not required for small
tortuous vessels where the gate encompasses a substantial number of vessels. The RI, PI
and PSV were calculated.
       The spatial peak temporal average intensity at the maximum amplitude and
minimum gate in simultaneous color and pulsed Doppler mode was approximately 90
mW/cm2, according to the manufacturer’s specification, which was well within the highest




                                                                                            6
limit recommended by the Bioeffects Committee of the American Institute of Ultrasound in
Medicine.
        For computer analysis of the data the program packages Statgraphics Version 4.0
(Statistical   Graphics   Corp.    Rockville,    USA,     1985-1989.     Serial   Number:
AG2068008214AR) and Statistica 6.0 (StatSoft Inc, Tulsa, USA, 1982-2002. Serial
number: AG2068008214AR) were used.
        Simple regression analysis was used to describe changes in Doppler indices with the
length of gestation. The Student t test was used to compare two variables. Multiple
regression was used to learn more about the relationship between several independent or
predictor variables and a dependent or criterion variable. A difference was considered
significant when p was less than 0.05.




                                                                                         7
Conclusions


       In Hungary, pulsed and color Doppler sonography was first applied to blood flow
investigation by the author, who was also the first to report his experience with this
imaging technology. In the present study, we analysed more than 7,500 pieces of data from
857 examinations performed between the 5th and the 40th weeks of gestation using pulsed
and color Doppler sonography. Features visualised by color Doppler imaging, as well as the
qualitative and quantitative characteristics of the Doppler waveforms produced by pulsed
Doppler were evaluated. From the Doppler indices, which can be measured and calculated,
resistance and pulsatility indices (RI and PI), peak systolic velocity [Peak Sys] and mean
velocity [TA peak] were applied to characterise the blood flow. Changes in uterine
vascularity and circulation were studied in normal and complicated pregnancies in
successive series of investigations.


       (1.) Investigations of uterine circulation in early normal pregnancies indicate that
main uterine arteries and their branches can be imaged with the help of TVCD and that
blood flow in various arteries can be isolated and investigated. The uterine artery and
intrauterine branches show different blood flow characteristics. Significantly lower
resistance and higher blood flow velocity can be detected in uterine arteries in early
pregnancies compared to non-gravid patients. Side differences can not be proved in either
case, which indicates symmetric uterine blood supply. Doppler indices of uterine branches
change in direct proportion with gestational age. Resistance indices decrease with
gestational age. Progressive fall in resistance to blood flow can be detected in intrauterine
branches from the main uterine artery towards spiral arterioles.


       (2.) In the case of ectopic pregnancy, blood flow in uterine arteries, tubal branches,
corpus luteum and transformed endosalpinx arterioles can be isolated and investigated with
TVCD. Depending on the color and pulsed Doppler sensitivity of the ultrasound
equipment, trophoblast flow can be imaged from 800-1,000 mIU/ml serum-βhCG level.
Trophoblast flow can be separated from corpus luteum flow on the basis of localisation,



                                                                                           8
appearance and blood flow values. Pregnancy implanting in the fallopian tube significantly
affects the blood supply of the tube concerned, thus it causes lateral displacement in uterine
circulation which normally has symmetrical blood supply. Side differences do not change
with gestational age. Uterine circulation and blood flow in the corpus luteum are
independent of time passed since the last menstruation.
       During ultrasonography of ectopic pregnancies, “snapshots” are taken of a
dynamically changing process showing either progression or degeneration at the particular
time of examination. Defining circulation characteristics increases diagnostic efficiency,
enabling selection of cases which need no invasive intervention, and plays an integral part
in determining the direction of complex investigations accompanying conservative or organ
retaining therapy.


       (3.) With an obstetric computer database, normal ranges of certain Doppler indices
were determined for uterine arteries, on the basis of an appropriate number of healthy
pregnant women between the 19th and 40th weeks of gestation. Investigations were
performed in regions, which are easy to identify with transabdominal color Doppler
imaging, and which serve as internationally accepted standard measurement points (uterine-
iliac “crossing”).
       It was determined that pulse Doppler waves in the main uterine branches show a
typical waveform change in the second half of normal pregnancy. Systolic peaks are
immediately followed by diastolic velocity plateau. Early diastolic “notch” which can be
revealed both in non-gravid patients and early pregnancies disappear on both sides by the
26th week of gestation. Doppler indices of the uterine arteries change with gestation.
Impedance indices decrease significantly, whereas velocity parameters increase
significantly with gestational age. The location of the placenta considerably affects blood
flow characteristics in the uterine arteries. The arteries closest to the placental bed have a
lower resistance and a higher velocity than the non-placental arteries on the opposite side.
Therefore, placental location must be taken into consideration for uterine blood flow
assessment. Mean circulation indices on both sides are suitable for assessment. Close




                                                                                            9
(negative) correlation can be revealed between resistance indices and velocity parameters in
uterine arteries. Resistance decreases while mean velocity increases.
       Resistance (RI and PI) and mean velocity are suitable for evaluation of the placental
bed and uterine branch perfusion. Definition of normal ranges served as a basis of
comparison for complicated pregnancies and as a starting point to decide to what extent the
investigation of uterine arteries supports the prediction of pathological conditions in clinical
practice.


       (4.) An intrauterine pregnancy was followed after bilateral hypogastric artery
ligature. It was determined that the ligature did not influence the blood flow in the uterine
arteries during pregnancy. Uterine arteries were visualised in their regular anatomic
positions and pulsed Doppler ultrasonography proved that the collateral artery network
does not only restore blood flow in uterine arteries, but it can also ensure increased blood
supply during pregnancy.


       (5.) On the basis of an obstetric computer database, characteristics of uterine artery
blood flow were analysed in patients with pre-eclampsia, gestational hypertension, and
normotensive pregnancies complicated by intrauterine growth retardation. Higher PI values
were observed in the uterine arteries of patients with pre-eclampsia, chronic hypertension
and normotensive pregnancies complicated with intrauterine growth retardation than in
normal pregnancies. Mean PI values of patients with pre-eclampsia, superimposed pre-
eclampsia and in pregnancies complicated with intrauterine retardation because of
abnormal placentation were higher than in the normotensive control group. The mean PI
value in the chronic hypertensive group was higher than in the normotensive group,
however, the difference was not significant. No significant differences in PI values could be
pointed out between groups with pre-eclampsia, superimposed pre-eclampsia and
normotensive pregnancies complicated with intrauterine retardation secondary to abnormal
placentation.




                                                                                             10
       (6.) It was concluded that marked changes can be identified in uterine artery blood
flow in pregnancies complicated with severe pre-eclampsia compared with normal
pregnancies. Qualitative and quantitative characteristics of pulse Doppler waves can be
different in the main uterine branches. The presence of a persistent early diastolic “notch”,
especially if bilateral, is a better independent indicator of pre-eclampsia than any other
Doppler parameter.
       Significantly increased resistance and decreased mean velocity in pre-eclampsia and
accompanying intrauterine retardation indicate decreased perfusion of the placental bed and
the entire uterine vascular system. In pre-eclampsia, strong negative correlation was found
between birth weight and uterine artery resistance indices. Due to the correlation between
intrauterine growth retardation and resistance values (RI and PI) outside the normal range,
the measurement of these indices makes the prediction of intrauterine growth retardation
possible.
       Results indicate that uterine artery blood flow investigation with color and pulsed
Doppler is suitable for assessing uterine perfusion and for making a prediction in
pregnancies complicated with pre-eclampsia and/or intrauterine growth retardation. In
comparison with normal pregnancies, changes are so marked that they make the prediction
of complications possible before symptoms and complaints manifest themselves. On the
basis of results published in the literature and the author’s conclusions, screening appears
worth considering in selected cases, e.g. in high-risk pregnancies, focusing on persistent
early diastolic “notch” in uterine arteries between the 24th and 26th weeks of gestation.


       The findings of this series of investigations clearly demonstrates the usefulness and
parameters of pulsed and color Doppler ultrasonography in the assessment of uterine
circulation in normal and complicated pregnancies. The investigation of uterine blood flow
is of great importance in ectopic pregnancies, pre-eclampsia and high risk pregnancies due
to toxemia as it provides particularly decisive information for clinical care.




                                                                                            11
Original publications of the author


1. Német J., Lipták M., Verebély T., Csabay L., Szabó I., Papp Z. (1992)
   Praenatalis ultrahang-diagnosztikai nehézséget okozó hydrocolpos esete.
   Gyermekgyógy. 43, 286-288.

2. Csabay L., Szabó I., Német J., Papp Z. (1992)
   Az embrió fejlődésének transvaginalis ultrahangvizsgálata koraterhességben
   (szonoembriológia) I. Az ébrény és mellékrészei.
   Lege Artis Medicinae 2, 512-517.

3. Csabay L., Szabó I., Német J., Papp Z. (1992)
   Az embrió fejlődésének transvaginalis ultrahangvizsgálata koraterhességben
   (szonoembriológia) II. Központi idegrendszer.
   Lege Artis Medicinae 2, 512-517.

4. Szabó I., Kádár K., Tóth Z., Kovács L., Német J., Csabay L., Papp Z. (1992)
   Intrauterin diagnosztizált multiplex intracardiális szívdaganat esete.
   Gyermekgyógy. 43, 282-285.

5. Szabó I., Csabay L., Német J., Papp Z. (1993)
   Transvaginalis színes Doppler-vizsgálat koraterhességben.
   Lege Artis Medicinae 3, 716-724.

6. Német J., Lipták M., Verebély T., Csabay L., Szabó I., Papp Z. (1993)
   Hydrocolpos.
   The Fetus 3, 1-4.

7. Szabó I., Csabay L., Németh J., Papp Z. (1993)
   Az uterus vérkeringésének transvaginalis színes Doppler ultrahangvizsgálata
   koraterhességben.
   Lege Artis Medicinae 3, 832-839.
8. Szabó I., Kádár K., Csabay L., Német J., Hajdú J., Papp Z. (1993)
   Komplex szívhibával szövődött teljes AV-blokk praenatalis nyomonkövetése.
   Lege Artis Medicinae 3, 930-935.

9. Inovay J., Szabó I., Csabay L., Szendei Gy., Papp Z. (1994)
   A méhen kívüli terhesség laparoszkópos kezelése salpingotomiával.
   Orv. Hetil. 135, 357-360.

10. Szabó I., Hajdú J., Marton T., Csabay L., Német J., Papp Z. (1994)
    Diaphragma defectus okozta non-immun hydrops.
    Gyermekgyógy. 45, 86-91.

11. Hajdú J., Szabó I., Szathmári A., Machay T., Koncz E., Papp Z. (1994)
    Komplex supraventricularis aritmia sikeres kezelése a 26. gesztációs héttől.
    Lege Artis Medicinae 4, 248-252.
12. Szabó I., Paulin F., Rigó J.Jr, Német J., Csabay L., Papp Z. (1994)
    Az arteria uterinák véráramlási jellegzetességei a normális terhesség második felében.
    Lege Artis Medicinae 4, 412-420.
13. Szabó I., Hajdú J., Csabay L., Német J., Papp Z. (1994)
    Magzati tachyarrhythmia praenatalis nyomon követése.
    Orv. Hetil. 135, 2603-2607.

14. Hajdú J., Marton T., Szathmári A., Sziller I., Machay T., Szabó I., Papp Z. (1994)
    Non-immun hydrops szindrómát okozó, praenatalisan diagnosztizált kettős üregű jobb
    kamra.
    Lege Artis Medicinae 4, 332-336.
15. Ádám Zs., Szabó I., Csabay l., Tóth-Pál E., Hajdú J., Német J. (1994)
    Kromoszóma-rendellenességekre gyanús ultrahangjelek a terhesség alatt.
    Lege Artis Medicinae 4, 602-607.

16. Szabó I. (1994)
    Color Doppler benignus nőgyógyászati kórképekben.
    Magy. Nőorv. L. 57, 391.

17. Inovay J., Szabó I., Csabay L., Szendei Gy., Papp Z. (1994)
    Laparoscopic management of ectopic pregnancy by salpingotomy.
    Acta Chir. Hung. 34, 315-322.

18. Paulin F., Szabó I., Rigó J. Jr. (1995)
    Doppler colour flow imaging of fetal intracerebral arteries and umbilical artery in the
    small for gestational age fetus
    Br. J. Obstet. Gynaecol. 102, 174.

19. Szabó I. (1995)
    Az ultrahang-diagnosztika lehetőségei a nőgyógyászatban.
    Praxis 4, 6-17.
20. Rigó J.Jr, Szabó I., Paulin F., Papp Z. (1995)
    Az arteria uterina pulzatilis indexe (PI) hypertoniával szövődött terhességekben.
    Magy. Radiol. 69, 1-4.
21. Hajdú J., Marton T., Tóth-Pál E., Szabó I., Machay T., Papp Z. (1995)
    Bal szívfél rendellenességek méhen belüli diagnosztikája.
    Orv. Hetil. 136, 2333-2337.

22. Papp Z., Sztanyik L., Szabó I., Inovay J. (1996)
    Successful pregnancy after bilateral internal iliac artery ligation monitored by color
    Doppler imaging.
    Ultrasound Obstet. Gynecol. 7, 211-212.

23. Hajdú J., Szabó I., Német J. (1996)
    Magzati supraventricularis tachycardia sikeres kezelése digoxin és amidaron
    kombinációjával.




                                                                                              13
   Orv. Hetil. 137, 2209-2211.

24. Hajdú J., Marton T., Tóth-Pál E., Német J., Szabó I., Papp Z. (1996)
    A jobb kamrai kiáramlás zavarainak intrauterin diagnózisa: Fallot-tetralogia,
    pulmonalis atresia kamrai septum defectussal, truncus arteriosus communis.
    Orv. Hetil. 137, 347-351.

25. Szabó I., Szánthó A., Német J., Csapó Zs., Szirmai K., Papp Z. (1996)
    A méh vérkeringésének színes Doppler vizsgálata endometriumcarcinomában.
    Lege Artis Medicinae 6, 714-721.

26. Szabó I., Szánthó A., Csapó Zs., Hidvégi J., Csabay L. (1996)
    Transvaginalis color Doppler ultrahangvizsgálattal korai stádiumban felismert
    elsődleges méhkürtrák.
    Magy. Radiol. 70, 166-168.

27. Patkós P., Csécsei K., Tóth-Pál E., Szabó I., Hruby E., Papp Z. (1996)
    Négyes ikerterhesség redukciója után kihordott kettős ikerterhesség.
    Orv. Hetil. 137, 2459-2463.

28. Hajdú J., Szabó I., Papp Cs., Görbe É., Papp Z. (1997)
    Ritmuszavar, mint a magzati echocardiográfia indikációja.
    Magy. Nőorv. L. 60, 11-15.

29. Szabó I., Szánthó A., Német J., Csapó Zs., Szirmai K., Papp Z. (1997)
    A myometrium inváziójának meghatározása endometrium-carcinomában transvaginalis
    ultrahangvizsgálattal.
    Orv. Hetil. 138, 1323-1327.

30. Szánthó A., Szabó I., Demeter A., Papp Z. (1997)
    A rosszindulatú petefészek-daganatos betegek ellátásának aktuális helyzete hazánkban.
    Orv. Hetil. 138, 405-411.

31. Beke A., Rigó J.Jr, Szabó I., Papp Z. (1997)
    Is there a fetal brain-sparing effect in pre-eclampsia?
    Ultrasound Obstet. Gynecol. 9, 429-429.

32. Hajdú J., Szabó I., Papp Cs., Görbe É., Ceskó I., Papp Z. (1997)
    Hemodinamikailag jelentős magzati ritmuszavarok kezelése.
    Orv. Hetil. 138, 2335-2338.

33. Szabó I., Csabay L. (1997)
    A Doppler keringésvizsgálatok jelentősége a szülészetben.
    Háziorv. Továbbképző Szle. 4, 295-299.

34. Csabay L., Szabó I. (1997)
    Az ultrahang-szűrés szerepe a terhesgondozásban.



                                                                                       14
   Háziorv. Továbbképző Szle. 4, 292-294.

35. Szabó I., Szánthó A., Papp Z. (1997)
    Uterine sarcoma: diagnosis with multiparameter sonographic analysis.
    Ultrasound Obstet. Gynecol. 10, 220-221.

36. Szabó I., Szánthó A., Csapó Zs., Csabay L., Szirmai K., Papp Z. (1997)
    A méhtestdaganatok véráramlási jellegzetességeinek vizsgálata színes Doppler-
    technikával.
    Lege Artis Medicinae 7, 718-726.

37. Tanyi J., Rigó J.Jr, Szabó I., Hariszti R., Szánthó A. (1997)
    Petefészek eredetű cystákkal szövődött terhességek.
    Orv. Hetil. 138, 2927-2930.

38. Belics Z., Csabay L., Szabó I., Joó J. (1997)
    Köldökzsinór cysta a terhesség első trimeszterében.
    Lege Artis Medicinae 7, 648-648.

39. Csabay L., Szabó I., Németh J., Papp Z. (1998)
    Az embryo fejlődésének transvaginalis ultrahangvizsgálata terhességben
    (sonoembryologia). A szikhólyag.
    Magy. Nőorv. L. 61, 125-132.

40. Csabay L., Szabó I., Papp Cs., Tóth-Pál E., Papp Z. (1998)
    Central nervous system anomalies.
    Ann. N. Y. Acad. Sci. 847, 21-45.

41. Szabó I., Csabay L., Tóth Z., Török O., Papp Z. (1998)
    Quality assurance in obstetric and gynecologic ultrasound: The Hungarian model.
    Ann. N. Y. Acad. Sci. 847, 99-102.

42. Hajdú J., Marton T., Papp Cs., Szabó I., Cesko I., Papp Z. (1998)
    A tricuspidalis atresia praenatalis diagnosztikája.
    Orv. Hetil. 139, 1219-1222.

43. Patkós P., Hruby E., Marton T., Hajdú J., Szabó I. (1998)
    Acardia (TRAP-sequentia).
    Orv. Hetil. 139, 1745-1749.

44. Csapó Zs., Szabó I., Tóth M., Dévényi N., Papp Z. (1999)
    Hyperreactio luteinalis in a normal singleton pregnancy. A case report.
    J. Reprod. Med. 44, 53-56.




                                                                                      15
45. Belics Z., Csabay L., Szabó I., Barakonyi E., Német J., Siposné Radványi Zs.,
    Pászkányné Jenei K., Hozsdora A. (2000)
    A medencecsontok (ossa ilii) által bezárt szög mérésének jelentősége Down-syndroma
    szűrésében.
    Magy. Nőorv. L. 63, 395-398.

46. Belics Z., Csabay L., Szabó I., Barakonyi E., Német J., Papp Z. (2000)
    Sonographic measurement of the fetal iliac angle as a marker for trisomy.
    Fetal Diagnosis and Therapy 15: 373-374.

47. Ujházy A., Szabó I., Csapó Zs., Papp Z. (2000)
    Achondrogenesis I. típus. Prenatalis diagnosztika az első trimeszterben
    Gyermekgyógy. 51, 48-53.

48. Szabó I. (2001)
    Váltsunk-e fogamzásgátlót?
    Praxis 10, 81-88.

49. Ujházy A., Szabó I., Csabay L., Marton T., Papp Z. (2001)
    Osteogenesis imperfecta praenatalis diagnosztikája a genetikai tanácsadás két évtizede
    során (1977-1999)
    Magy. Nőorv. L. 64, 235-240.

50. Szánthó A., Szabó I., Csapó Zs., Bálega J., Demeter A., Papp Z. (2001)
    Assessment of myometrial and cervical invasion of endometrial cancer by transvaginal
    sonography
    Eur J Gynaec Oncol 22: 209-212.

51. Szabó I., Szánthó A., Csabay l., Csapó Zs., Szirmai K., Papp Z. (2002)
    Color Doppler ultrasonography in differentiation of uterine sarcomas from uterine
    leiomyomas
    Eur J Gynaec Oncol 23: 29-34.

52. Szabó I., Csabay L., Belics Z.. Fekete T., Papp Zoltán (2002).
    A méh vérkeringésének transvaginalis színes Doppler ultrahangvizsgálata méhen kívüli
    terhességben
    Magy. Nőorv. L. 65, 259-265.

53. Szabó I., Csabay L., Belics Z., Fekete T., Papp Z.
    Assessment of uterine circulation in ectopic pregnancy by transvaginal color Doppler
    Eur J Obst Gyn Reprod Biol (Közlésre elfogadva 2002)

54. Belics Z., Csapó Zs., Szabó I., Pápay J., Szabó J., Papp Z.
    A large gastrointestinal stromal tumor presenting as an ovarian tumor




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   J Reprod Med (Közlésre elfogadva 2002)

55. Belics Z., Beke A., Csabay L., Szabó I., Papp Z.
    Sonographic measurement of the fetal iliac angle in trisomy 21, 18 and 13
    Fetal Diagnosis and Therapy (Közlésre elfogadva 2002)

Chapters:

1. Paulin F., Szabó I., Rigó J.jr, Papp Z. (1993)
   Improved prediction of IUGR using ratios of blood flow parameters measured by color
   Doppler equipment
   In: Perinatal Medicine Eds. E.V. Cosmi, G.C. Di Renzo
   Monduzzi Editore, Bologna, 943-946.

2. Szabó I., Papp Z. (1995)
   Doppler flowmetria (26. fejezet), Egyéb craniospinalis rendellenességek (55. fejezet)
   In: Klinikai Genetika, Szerk. Papp Z.
   Golden Book Kiadó, Budapest, 277-287., 515-522.

3. Szabó I., Csabay L., Német J., Papp Z. (1996)
   Transvaginal color Doppler for assessment of uterine tumour vascularity
   In: Doppler in Gynaecology and Infertility Eds. Kurjak A, Kupesic S.
   CIC Edizioni Internazionali, Roma, 164-173.

4. Szabó I. (1997)
   A női kismedence transabdominalis és transvaginalis ultrahangvizsgálata. A női
   kismedencei szervek duplex ultrahangvizsgálata (4.2 - 4.4 fejezet). Terhességi
   transvaginalis ultrahangvizsgálat. Terhességi transabdominalis ultrahangvizsgálat
   Folliculometria ultrahangmódszerrel. A magzati és a lepényi keringés duplex
   ultrahangvizsgálata (5.1 - 5.6 fejezet). Ultrahangvezérelt nőgyógyászati beavatkozások,
   Ultrahangvezérelt terhességi beavatkozások (10.7 - 10.8 fejezet).
   In: Hogyan vizsgáljunk ultrahanggal? Szerk. Harkányi Z.
   Literatura Medica Kiadó, Budapest, 68-73., 84-97., 132-135.
5. Szabó I., Papp Z. (1999)
   Fetomaternal transfusion: state of the art
   In: Fetal Medicine, Eds. Chervenak F.A., Kurjak A.
   The Parthenon Publishing Group, New York, 211-216.

6. Szabó I. (2001)
   Jó- és rosszindulatú kismedencei tumorok (30. fejezet)
   In: Szülészet-Nőgyógyászati Ultrahang-Diagnosztika, Szerk. Tóth Z. és Papp Z.
   White Golden Book Kiadó, Budapest, 356-375.

7. Szabó I. (2001)
   Terhesség (3.18. fejezet)
   In: Ultra-Szonográfia, Szerk. Harkányi Z. és Morvay Z.
   Minerva Kiadó, Budapest, 179-185.




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8. Jakab Zs., Szabó I. (2001)
   Vérzészavarok (3.17. fejezet)
   In: Ultra-Szonográfia, Szerk. Harkányi Z. és Morvay Z.
   Minerva Kiadó, Budapest, 169-178.

9. Szabó I. (2002)
   A női kismedence ultrahangvizsgálata
   In: Belgyógyászati Ultrahangdiagnosztika, Szerk. Szebeni Á.
   Medicina Könyvkiadó, Budapest, 193-215.

Abstracts:

1. Szabó I., Csabay L., Német J., Papp Z. (1992)
   Follow-up of the intrauterine condition of a fetus with ventricular septum defect
   complicated with total AV block
   Fetal Diagnosis and Therapy 7, (Suppl 1.) 40.
2. Szabó I., Csabay L., Német J., Papp Z. (1993)
   Transvaginal color Doppler study of blood flow in ectopic pregnancies
   Ultrasound Obstet Gynecol 3, (Suppl. 1) 43.

3. Csabay L., Szabó I., Német J., Papp Z. (1993)
   Diagnostic value of transvaginal sonography in early detection of different types of
   ectopic pregnancies
   Ultrasound Obstet Gynecol 3, (Suppl. 1) 39.

4. Szabó I., Csabay L., Német J., Papp Z. (1994)
   The assessment of pelvic blood flow by transvaginal color Doppler in ectopic and
   intrauterine pregnancies
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 61.

5. Inovay J., Csabay L., Szabó I., Német J., Sipos Zs., Papp Z. (1994)
   The role of color Doppler transvaginal ultrasound velocimetry and serial beta-hCG
   estimation in the expectant management of ectopic pregnancy (a case report with long-
   term follow up of the patient)
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 62.
6. Tóth-Pál E., Nagy J., Német J., Szabó I., Csabay L., Papp Z. (1994)
   Ultrasonographically detectable markers indicating fetal karyotyping
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 63.

7. Szabó I., Szánthó A., Német J., Ádám Zs., Papp Z. (1994)
   The assessment of ovarian tumor vascularity and blood flow characteristics by
   transvaginal color Doppler
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 67.

8. Szánthó A., Szabó I., Német J., Ádám Zs., Papp Z. (1994)
   Transvaginal color Doppler for assessment of uterine tumor vascularity
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 68.




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9. Német J., Szabó I., Csabay L., Papp Z. (1994)
   Measurement of scar thickness after Cesarean section using ultrasound
   Ultrasound Obstet Gynecol 4, (Suppl. 1) 74.
10. Paulin F., Szabó I., Rigó J., Papp Z. (1994)
    SGA or LBW fetuses are better predicted by the cerebral-uterine Doppler ratios?
    Ultrasound Obstet Gynecol 4, (Suppl. 1) 118.

11. Beke A., Szabó I., Takács Gy., Fedák L., Papp Z. (1994)
    Effect of the epidural anesthesia on the uteroplacental blood flow
    Ultrasound Obstet Gynecol 4, (Suppl. 1) 119.

12. Csabay L., Beke A., Szabó I., Baksa J., Tóka M., Papp Z. (1994)
    Fetal intraventricular hemorrhage diagnosed during the third trimester of pregnancy
    Ultrasound Obstet Gynecol 4, (Supp 1) 164.
13. Ádám Zs., Bardóczy Zs., Tóth-Pál E., Német J., Szabó I., Csabay L., Papp Z. (1994)
    Autosomal dominant polycystic kidney disease: genetic counselling and prenatal
    ultrasound diagnosis
    Ultrasound Obstet Gynecol 4, (Suppl. 1) 175.

14. Marton T., Hajdú J., Szabó I., Tóth-Pál E., Szende B., Papp Z. (1994)
    Prenatal diagnosis of left ventricular malformations
    Ultrasound Obstet Gynecol 4, (Suppl. 1) 176.

15. Hajdú J., Szabó I., Tóth-Pál E., Silhavy M., Szabó M., Machay T., Papp Z. (1994)
    Hemodynamic changes in anemic fetuses
    Ultrasound Obstet Gynecol 4, (Suppl. 1) 204.

16. Szabó I., Csabay L., Német J., Papp Z. (1995)
    Evaluation of the uterine vascularity by color Doppler ultrasonography in endometrial
    cancer
    Ultrasound Obstet Gynecol 6, (Suppl. 2) 73.
17. Hajdú J., Szabó I., Görbe É., Papp Z. (1995)
    Arrhythmia as an indication for fetal echocardiography
    Ultrasound Obstet Gynecol 6, (Suppl. 2) 101.
18. Szendei Gy., Dévényi N., Szabó I., Inovay J., Papp Z. (1996)
    Diagnosis and hormonal treatment of endometriosis
    Gynecol Endocrinol 10, (Suppl. 4) 171.

19. Szánthó A., Szabó I., Papp Z. (1997)
    Assessment of myometrial invasion in endometrial cancer by transvaginal
    ultrasonography
    Eur J Gynaecol Oncol 18(4), 251.

20. Szabó I., Szánthó A., Csabay L., Papp Z. (1997)
    Transvaginal color Doppler for assessment of uterine vascularity in cases of uterine
    fibroids and sarcomas




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   Ultrasound Obstet Gynecol 7, (Suppl. 1) A 121.

21. Szánthó A., Szabó I., Demeter A., Papp Z. (1999)
    Clinical experience with uterine sarcomas: sonographic characteristics and treatment
    Int J Gynecol Cancer, 9, (Suppl. 1) 142 (F127).

22. Szabó I. (2000)
    Assessment of uterine vascularity in endometrial cancer
    Ultrasound Obstet Gynecol 16, (Suppl. 1) 12: WS05-4.

23. Belics Z., Csabay L., Beke A., Szabó I., Papp Z. (2002)
    Sonographic measurement of the fetal iliac angle: a new marker for the prenatal
    detection of trisomy 21?
    Fetal Diagnosis and Therapy 17, (Suppl. 1) 67.
24. Szabó I. (2002)
    Fetal arrhythmia, follow up of the intrauterine condition
    Fetal Diagnosis and Therapy 17, (Suppl. 1) 126.

25. Fekete T., Tóth Z., Szabó I., Csabay L., Papp Z. (2002)
    Quality control in prenatal ultrasonography in Hungary
    Fetal Diagnosis and Therapy 17, (Suppl. 1) 184.




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