Document 6428606

Archives of Perinatal Medicine 15(4), 202-208, 2009
ORIGINAL PAPER
Doppler assessment of blood flow
in selected blood vessels in TTTS
MARIOLA ROPACKA-LESIAK, WIESŁAW MARKWITZ, GRZEGORZ H. BRĘBOROWICZ
Abstract
The pathophysiology of twin-to-twin transfusion syndrome (TTTS) is linked to the presence of vascular
anastomoses between two fetal circulations. Aim of the study: The aim of the study was to estimate the value of
Doppler flow analysis in the prediction of abnormal fetal outcome or death of the fetus in the pregnancies
complicated by TTTS. Material: The study included 54 twins from TTTS pregnancies. Results: Abnormal UAPI,
the centralization phenomenon and ARED flow were observed in the smaller fetus, whereas the abnormal PIMCa
in the larger one. Conclusion: Simultaneous monitoring of the blood flow in the umbilical artery and middle
cerebral artery have the greatest predictive value in the prognosis of the fetal outcome.
Key words: twin pregnancy, TTTS, Doppler analysis
Twin-to-twin transfusion syndrome (TTTS) occurs
almost exclusively in monochorionic pregnancies (MC).
MC twins account for about 70% of monochozygotic
twins (MZ). 15-20% of MC pregnancies develop the chronic form of TTTS [16, 20, 21]. Pathophysiology of TTTS
is linked to the presence of vascular anastomoses
between two fetal circulations. Vascular anastomoses are
common in monochorionic placentas. The occurrence of
unidirectional arterio-venous anastomosis (A-V) in the
absence of bi-directional compensatory arterio-arterial
anastomosis (A-A) suggests poor prognosis for the fetus.
Other abnormalities are related to unequal placental
sharing. Until recently, little or no attention has been
paid to this phenomenon. Currently it is believed that it
is as essential as the presence of anastomosis itself. The
degree of asymmetry (60 : 40, 70 : 30, etc.) can have
a significant effect on the appearance of placental insufficiency of one of the fetuses, and clinical manifestation
may vary, depending on gestational age or type and
number of vascular anastomoses. In the absence of A-A
anastomosis, asymmetric placental sharing may cause
growth restriction in MC pregnancies. Bidirectional anastomosis may be the only chance for the fetus, which
uses a small area of placental exchange, which in turn
provides him with additional nutrients and assures adequate oxygenation of the fetus. This complex system of
vascular connections, together with placental symmetry
or asymmetry, are responsible for the hemodynamic
balance and the received Doppler findings [19].
If in the placenta there are only arterio-arterial,
and/or veno-venous connections. Blood flow between the
fetuses, due to identical dominant resistance in these
vessels and a relatively large diameter of the lumen,
should theoretically take place in any direction, depending on fetal intravascular pressure and incidence of fetal
heart rate, not causing any hemodynamic disequilibrium.
Any hemodynamic imbalance in one of the fetuses may
cause almost instantaneous blood flow from/to the other
fetus. Intrauterine development of both fetuses might be
symmetric only on condition that, under physiological
conditions, blood pressure is similar in the umbilical vessels of both twins. So far, however, this theory has not
been sufficiently confirmed [1]. There is a strong likelihood that direction and magnitude of blood flow may be
affected by: different diameters of the vessels making
the connections, length of the vessel (measured from
the umbilical cord to the junction) and the angle at
which these vessels are linked together. Also, vessels
which form a direct vascular connection and run on the
surface of fetal placenta, may be influenced by intraamniotic pressure, especially in case of acute polyhydramnion.
In the diagnosis of TTTS, Doppler studies are as
vital and important as standard ultrasound. The study of
blood flow velocimetry in fetal vessels, such as umbilical
artery and vein, middle cerebral artery and ductus
venous, provide valuable information about the existing
hemodynamic disturbances. Fetal echocardiography is
particularly useful in the assessment of the cardiovascular system of the ‘recipient’, often showing features of
cardiovascular dysfunction. Doppler blood flow velocimetry found its application in differentiating the characteristics of fetal intrauterine growth restriction in genetics and in the course of placental insufficiency [8]. Its
Department of Perinatology and Gynecology, Medical University in Poznań
Doppler assessment of blood flow in selected blood vessels in TTTS
inclusion in the diagnosis of discordant fetal growth in
multiple pregnancy seems appropriate and justified.
TTTS is one of the reasons for discordant fetal growth.
Various Doppler results, often ambiguous and incomparable, have often been observed in TTTS. This is mainly
due to different diagnostic criteria and various stages of
the disease. Some authors marginalize the importance
of Doppler studies in TTTS [14, 15], whereas many
others underline their importance [3, 12, 17, 18].
Materials and methods
The study included 54 twins from TTTS pregnancies, who were hospitalized in the Gynecology and Obstetric Clinical Hospital in Poznań. Maternal age ranged
from 18 to 37 years. Analysis of blood flow in selected
arterial vessels, i.e. in umbilical artery (UA) and middle
cerebral artery (MCA), has been performed. The predictive value of blood flow analysis has been assessed in
order to predict abnormal fetal outcome and intrauterine
or neonatal death in TTTS.
Doppler studies were performed either once or repeatedly, with the last one taking place no later than 7
days before delivery. The analysis included the result of
the last survey before delivery. Duration of pregnancy
was calculated on the basis of last menstrual period or
ultrasound in the first trimester of pregnancy, together
with the date of first fetal movements.
The study was conducted using VOLUSON 730
EXPERT with the variable-frequency 3.5 and 5.0 MHz
transducer, operating in real time with the option of
pulse wave and color Doppler. During the examination
the pregnant woman adopted a reclining position,
slightly on the left side, to avoid hemodynamic changes
caused by pressure on the inferior vena cava. Time of
examination did not exceed 15-30 minutes. All Doppler
studies were performed during the immobility of the
fetus and in the absence of respiratory activity of the
fetus and the pregnant woman. Blood flow was assessed
on the basis of pulsatility index (PI) according to Gosling
[9]. Coefficient was calculated on the basis of the average value of at least three good-quality consecutive
curves which characterize blood flow. PI values above 95
percentile for the given gestational age were considered
abnormal. Absent or reversed end-diastolic flow were
determined as ARED.
Similarly, evaluation of blood flow in the middle
cerebral artery was carried out in the same group of
patients. PI values below 5 percentile for that gestational
age were considered abnormal. The ‘brain sparing’ effect
was defined on the basis of cerebro-umbilical ratio (PI
203
ratio). Cerebro-umbilical ratio was defined according to
Gramellini [10], calculating the ratio of PI MCA/ PI UA.
The value less than 1.08 was assumed to be abnormal
(brain sparing effect).
The incidence of abnormal Doppler results in the UA
and the MCA, ‘brain sparing’ effect and the presence of
ARED in the larger and smaller twin were compared.
Next, Doppler results were correlated with fetal/newborn outcome and/or death. In addition, assessment of
the prognostic value of Doppler studies in relation to the
fetal outcome was performed.
Results
The study was conducted in a group of 54 twins from
27 pregnancies complicated by TTTS. 70.3% were found
to have discordant fetal growth, 51.9% presented abnormal umbilical cord attachment. Mean gestational age
at delivery was 32.4 weeks, and perinatal mortality
reached 44.4%. In many cases abnormal Doppler blood
flow velocimetry in the umbilical artery and middle cerebral artery were observed (42.6% and 24.5% respectively). Table 1 summarizes the characteristics of the study group.
Table 1. Characteristics of the study group
Age of pregnant woman (years)
Gestational age at delivery (weeks)
28.5(18-37)
32.4 ± 2.9
Primipara (%)
55.6
PI UA abnormal result (%)
42.6
PI MCA abnormal result (%)
24.5
ARED (%)
25.9
Brain sparing effect (%)
39.6
Growth discordance:
< 15.0% (%)
$ 15.0 % (%)
29.7
70.3
Abnormal umbilical cord attachment (%)
51.9
Death (%)
44.4
Table 2 illustrates the incidence of abnormal Doppler findings in a larger (L) and smaller (S) fetus, together with the assessment of fetal outcome. Analysis of
the results showed no statistically significant differences
between larger and smaller fetuses in the chosen parameters, except for the presence of abnormal umbilical
cord attachment, which was significantly more often
observed in the smaller twin. Abnormal UA PI, the
centralization phenomenon and ARED phenomenon
were observed more frequently in the smaller twin,
whereas the abnormal PI MCA in the larger one. How-
204
M. Ropacka-Lesiak, W. Markwitz, G.H. Bręborowicz
ever, the differences between the fetuses were not statistically significant.
Table 2. Comparison of abnormal Doppler findings
incidence and fetal outcome in TTTS
B
S
p
UA (%)
29.6
55.6
NS
MCA (%)
25.9
22.2
NS
ARED (%)
18.5
33.3
NS
Brain sparing (%)
29.6
48.1
NS
Ap 1’(median)
5
4
NS
Ap 5’(median)
7
8
NS
Ap 5’ < 7 (%)
40.9
22.7
NS
Abnormal PI values:
pH*
7.29 ± 0.11 7.27 ± 0.13
NS
pH < 7.20 (%)
22.7
22.7
NS
Death (%)
48.1
40.7
NS
Abnormal umbilical
cord attachment (%)
22.2
91.0
< 0.001
(n = 22) – intrauterine deaths were excluded from the analysis
Table 3. Abnormal blood flow in the umbilical artery and middle
cerebral artery in correlation with fetal or neonatal death
Fetal or neonatal
death
p
(+)
n = 24
(!)
n = 30
PI UA abn. (%)
33.3
50.0
NS
PI MCA abn. (%)
17.4
30.0
< 0.001
Brain sparing effect (%)
34.8
43.3
NS
PI UA abn.
and/or PI MCA abn. (%)
39.1
50.0
NS
abn. – abnormal result
Table 3 shows the incidence of abnormal Doppler
findings in relation to intrauterine or neonatal death.
There were no statistically significant differences in the
parameters analyzed apart from abnormal blood flow in
the middle cerebral artery. An explanation for this phenomenon may be the loss of mechanisms responsible for
the contraction in vascular bed after compensatory mechanisms have been lost in cases of significant fetal
distress. Reduction in vascular resistance in cerebral
circulation is one of the compensation mechanisms in
states of deprivation of the fetus. Prior to fetal death,
adaptability may be lost and narrowing of the vascular
bed may occur, which is associated both with the change
in vascular sensitivity to hypoxia and the reduction of
cardiac output.
Table 4 shows an increase of abnormal Doppler
findings in cases of abnormal fetal outcome with the
exception of the middle cerebral artery. Reduction of
vascular resistance in cerebral circulation correlated less
frequently with abnormal fetal outcome, which may be
associated with an increase in vascular resistance in
cases of severe fetal hypoxia.
Table 4. Correlation of abnormal fetal outcome with abnormal
PI values in umbilical artery and middle cerebral artery
Fetal outcome
normal
(n = 22)
abnormal
(n = 32)
p
PI UA abn. (%)
40.9
43.8
NS
PI MCA abn. (%)
27.3
22.6
< 0.001
Centralization (%)
31.8
45.2
NS
PI UA abn. and/or PI
MCA abn. (%)
40.9
48.4
NS
abn. – abnormal result
Table 5. Predictive value of blood flow in the umbilical and middle cerebral artery in predicting abnormal fetal outcome
and intrauterine or neonatal death in TTTS
Sensitivity (%) Specificity (%) PPV (%) NPV (%)
LR
OR
Death prediction
PI UA abn.(%)
33.3
50.0
34.8
48.4
0.7
0.5(0.2-1.5)
PI MCA abn. (%)
17.4
30.0
16.0
32.1
0.2
0.09(0.02-0.3)
Centralization (%)
34.8
43.3
32.0
46.4
0.6
0.4(0.1-1.2)
PI UA and/or PI MCA abn. (%)
39.1
50.0
37.5
51.7
0.8
0.6(0.2-1.9)
PI UA abn. (%)
40.9
45.2
34.6
51.9
0.7
0.6(0.2-1.7)
PI MCA abn. (%)
27.3
22.6
20.0
30.4
0.3
0.1(0.03-0.4)
Centralization (%)
31.8
45.2
29.2
48.3
0.6
0.4(0.1-1.2)
PI UA abn. and/or PI MCA abn. (%)
40.9
48.4
0.36
53.6
0.8
0.6(0.2-1.9)
Prediction of newborn status
Doppler assessment of blood flow in selected blood vessels in TTTS
However, almost none of the examined parameters, except the middle cerebral artery, showed any statistical
significance.
Simultaneous monitoring of the blood flow in the
umbilical artery and middle cerebral artery showed the
greatest sensitivity, specificity, PPV and NPV in forecasting abnormal fetal outcome or death of the newborn.
However, with regard to the odds ratio, assessment of
blood flow in these vessels did not show statistical significance in the analyzed parameters. Analysis of prognostic value is shown in table 5.
205
of blood flow during atrial systole and abnormal pulsations in the umbilical vein is particularly interesting. The
signal was obtained from fetal umbilical vessels of the
smaller twin (donor) in TTTS.
Fig. 2 and 3 illustrate the standard curves for the
coefficients of PI UA and PI MCA, with superimposed PI
values obtained from twin pregnancies complicated by
TTTS.
3,0
PI TŚM W
PI TŚM M
median
5-95 percentile
2,8
PI – middle cerebral artery
2,6
2,4
2,2
2,0
1,8
1,6
1,4
1,2
1,0
Fig. 1. Abnormal blood flow waveforms in the umbilical artery
with the absence of end-diastolic flow. Pulsatile flow in the
umbilical vein is presented underneath
3,0
PI – umbilical artery
PI TP W
PI TP M
median
5-95 percentile
1,5
1,0
0,5
22
24
26
28
30
32
34
36
38
week of pregnancy
Fig. 3. PI MCA values in TTTS
Discussion
2,5
2,0
0,8
22
24
26
28
30
32
34
36
38
week of pregnancy
Fig. 2. PI UA values mirroring vascular resistance in TTTS
Fig. 1 illustrates the abnormal shape of the waveforms in the umbilical artery, also known as ARED. Lack
Transfusion syndrome is a complication of multiple
monochorionic pregnancies. Development and the
course of TTTS depend mainly on the type, size and
number of vascular anastomoses, development and size
of the placenta and functional division of the placenta
sharing, concentration of proteins in the blood serum of
the fetus, as well as the presence of polyhydramnios/
oligohydramnios, leading to pressure vessels in the
placenta. A complex, sometimes very complex, network
of vascular connections, exists in monochorionic placentas and it may be responsible for the diversity of the
observed Doppler findings. A group of 54 twins from 27
pregnancies complicated by the TTTS syndrome was
analyzed in the presented study. The study group was
characterized by low gestational age at delivery (32.4
weeks). In 70.3% of cases discordant fetal growth was
found, in 51.9% of cases abnormal umbilical cord attachment was observed, and fetal and infant mortality
amounted to 44.4% (table 1). According to literature fetal mortality data in untreated TTTS reaches 80-100%.
206
M. Ropacka-Lesiak, W. Markwitz, G.H. Bręborowicz
Amnioreduction or laser therapy reduces mortality to 4050% [5]. In many cases abnormal Doppler blood flow
spectra in the UA and MCA were found. Analysis of the
incidence of abnormal Doppler findings in the larger and
smaller infant showed statistical differences, with the
exception of the higher frequency of abnormal attachment of the umbilical cord in the smaller fetus (table 2).
Although the differences did not show statistical significance, an increased incidence of abnormal PI values in
UA, and the brain sparing effect, as well as ARED
phenomenon in the smaller fetus, are particularly worth
noting. Absent or reversed end-diastolic flow in the UA
is commonly regarded as the exponent of high vascular
resistance and unfavorable prognosis for the fetus [2, 7,
22]. Bruner also showed increased incidence of elevated
vascular resistance, abnormal attachment of the
umbilical cord and fetal microcirculation disturbances in
the placenta [4]. Similarly, Taylor et al., found increased
incidence of abnormal Doppler findings in the UA in the
smaller fetus (‘donor’) [24].
In the following work we have analyzed and investigated the relationship between the Doppler results and
the fetal outcome. In the group of intrauterine or neonatal deaths there were no differences between the
analyzed parameters except for the MCA (table 3). An
explanation of this phenomenon, in relation to the
changes observed in the umbilical artery, may be higher
frequency of medical interventions (cesarean sections)
to prevent fetal death and(or) not sensitive enough
assessment of the blood flow in this vessel due to the
pathomechanism observed in this syndrome. The abovementioned has been confirmed in the articles and research which showed a stronger correlation of blood
flow disturbances in venous and intracardiac blood flow
with fetal and neonatal death [22]. Therefore, PI measurements in the umbilical artery do not reveal cardiovascular disorders, such as hypervolemia which is characteristic for this syndrome. With regard to the MCA, loss of
self-regulatory mechanisms (resulting from the progressive damage to the fetus) may play a significant role,
together with constriction of vascular bed, which manifests itself as an apparently normal values of the PI,
being in fact an exponent of exhausted compensatory
mechanisms. This is connected with both a change in
vascular sensitivity to hypoxia and the reduction of
cardiac output. Similar results were obtained by analyzing abnormal blood flow in the MCA in correlation with
abnormal fetal outcome. Other parameters characterizing the abnormal blood flow in the test vessels were
observed more frequently in twins whose condition after
birth was abnormal (table 4). These results did not differ
statistically. Simultaneous monitoring of the blood flow
in the UA and MCA revealed the highest sensitivity in
predicting abnormal fetal/neonatal outcome or death
(39.1% and 40.9% respectively) (table 5). The obtained
results, relatively low sensitivity, specificity (50% and
48.4%), PIP (37.5% and 36.0%) and NPV (51.7% and
53.6%), have a relatively weak prognostic value of the
investigated method. Findings of Taylor et al, are particularly interesting as they showed that abnormal blood
flow in UA in a smaller fetus with a pulsatile flow in
a fetal UV, together with the lack of possibility to visualize prenatal A-A anastomosis, are strong exponents
of adverse fetal outcome [25]. The results presented in
table 4 and 5 refer to both fetuses, while Taylor analyzed
the ARED phenomenon only in the smaller fetus (the
donor). His group was similar, involving 23 pairs of
twins. Assessment of blood flow in the UA of the smaller
fetus may theoretically have a better prognostic value,
since the mechanism of observed abnormalities in the
fetus concerns mainly hypervolemia and anemia and is
similar to those observed in the course of placental
insufficiency. Moreover, the fact that Taylor included in
his analysis only the ARED phenomenon, which is an
extreme form of abnormal blood flow disturbances, may
significantly increase the sensitivity of the test.
Hecher et al. presented interesting findings concerning the assessment of cardiovascular hemodynamics in
fetuses with TTTS syndrome in the second trimester of
pregnancy [12]. An increase in vascular resistance in UA
in both ‘recipient’ and ‘donor’ was noted. Below 21 t.c.
concerned only ‘the recipient’. In our studies the increased vascular resistance in UA was observed in both
the major (‘recipient’) and the smaller fetuses (‘donor’)
(table 3, fig. 1, 2). The pressure of placental vessels or
umbilical cord (in the case of membranous attachment)
as a result of intraamniotic pressure increase in polyhydramnion, as a result of intraamniotic pressure, may
be the explanation for the high vascular resistance in the
recipient. Another explanation is the development of
edema in the placenta by congestive heart failure in the
course of cardiovascular hypervolemia. The increase in
vascular resistance in the UA of the ‘donor’ occurs most
likely due to originally impaired placental development
or umbilical cord compression caused by polyhydramnios in the bag of the ‘recipient’. The ‘donor’ is usually
exposed to severe placental insufficiency, often further
complicated by chronic bleeding to the circulation of the
‘recipient’, the consequence of which is the development
of hypervolemia. In the MCA of the ‘donor’, Hecher
Doppler assessment of blood flow in selected blood vessels in TTTS
observed both an increase in the PI, probably as a result
of high pressure on head following polyhydramnios in
the amniotic sack of the ‘recipient’, as well as the
reduction of PI as a result of anemia and hypoxia.
Similarly, in the presented work the reduction of
vascular resistance in the MCA was observed in both the
smaller and larger fetus. Increase in vascular resistance
was not the subject of analysis in this work. Correct
values of the PI values at a time when there were no
redistribution of the circulatory system have often been
observed. Hecher et al. often observed in the ‘recipient’
reduced values of the PI in the MCA. Reduction in
vascular resistance in this vessel may be the consequence of cardiac failure in the course of hypervolemia
(decrease in cardiac output) and the extension of the
vascular bed following hypoxia. Other researchers have
also pointed to increased resistance in the presence of
UA of the smaller twin in TTTS. ARED phenomenon has
been linked with unfavorable prognosis for the fetus
[26]. Using Doppler angiography Haberman et al. observed abnormal placental blood flow in the smaller
fetus, with intrauterine growth restriction and oligohydramnios [11].
Gaziano, comparing a group of MCDA and DCDA
fetuses with low birth weight, observed that in the first
group the signs of brain sparing effect occurred significantly more often [6]. It is very likely that vascular
connections in the placenta are responsible for that fact,
as well as hemodynamic disturbances they have caused.
Ohno et al. suggest that Doppler blood flow measurements in the UA may be useful in prediction of generalized edema development. The usefulness of Doppler
ultrasound in the monitoring of fetomaternal hemodynamics and fetal well-being, particularly in the course of
therapy, has also been confirmed. However, no benefit
was found with regard to the fetus [17]. Rizzo et al. have
voiced the problem of limited application of this technique for the early diagnosis of TTTS [18].
Only a few authors have noted the lack of circulatory
centralization in pregnancies complicated with TTTS.
Suzuki et al. assessed blood flow in the MCA and UA in
fetuses with intrauterine growth restriction in cases
complicated and not complicated by TTTS [23]. They
found significantly higher PI values in the MCA in the
group of fetuses with TTTS. Even more pronounced increase in the PI ratio was observed in fetuses with
features of periventricular leucomalatia. Their observations suggest the absence of the brain sparing phenomenon, which is frequently observed in fetuses from restricted growth group and in cases of hypoxia due to
207
placental insufficiency [23]. PI values in the UA of the
smaller twin were significantly higher in the group with
TTTS compared to the group without the symptoms of
this syndrome. These values are lower after amnioreductions, what might be a sign of improved cardiovascular
hemodynamics. An increase of the PI value in the MCA
some of the ‘donors’ was explained by fetal head compression as a result of polyhydramnios in the ‘recipient’
sac and reduction of the volume of left ventricular ejection with subsequent decompensation of cerebral circulation.
Rizzo et al. analyzed differences in the PI values in
the fetal circulation in pairs of twins with discordant
growth in cases of placental insufficiency or TTTS [18]
and noticed the presence of various Doppler results, depending on different pathomechanisms underlying
observed abnormalities. Serial blood flow studies in a larger, properly developing twin, demonstrated lack of any
differences compared to the results obtained in fetuses
with uncomplicated single pregnancies. Conversely, the
smaller twin showed progressive changes in Doppler
indices, similar to changes observed in fetuses with
limited growth in a single pregnancies. These changes
included a progressive increase in the PI in the UA and
the descending aorta in the period before symptoms of
fetal distress. Often it was accompanied by a reduction
of PI in the middle cerebral artery. It was suggested that
Doppler indices of the smaller twin or Doppler indices
differences in pairs, may be useful in predicting fetal
distress [13]. Vetter suggested that the assessment of
blood flow in vessels can be a good indicator of the proper function of the placenta, allowing to assess the redistribution of the circulation which is associated with
a threat to fetal life [27]. Jensen correlated RI differences in UA in 25 pairs of twins with pO2 differences,
showing that gas exchange in the placenta was impaired,
when the resistance in UA increased [15].
This diversity of results presented by the abovementioned authors may result, first of all, from heterogeneous definitions and criteria used in the diagnosis of
TTTS. Secondly, compared groups are usually too small
due to the relatively rare occurrence of this complication. Thirdly, Doppler results may be affected by the
existence of different pathomechanisms responsible for
the observed changes in this syndrome. Fourthly, a definite influence is associated with complex and very diverse network of vascular connections in the placenta.
Finally, the extent of hemodynamic disturbances has
major impact on the obtained results.
The work done under the grant KBN 2PO5E 030 27
208
M. Ropacka-Lesiak, W. Markwitz, G.H. Bręborowicz
References
[1] Blickstein I. (1990) The twin-twin transfusion syndrome.
Obstet. Gynecol. 76: 714-722.
[2] Bręborowicz G.H., Dubiel M., Szpurek D. et al. (1994)
Wartość prognostyczna zaniku lub odwrócenia końcoworozkurczowego przepływu krwi w tętnicy pępowinowej
w diagnostyce zagrożenia płodu. Gin. Pol. 65: 341-345.
[3] Bręborowicz G.H., Ropacka M., Markwitz W. (2002) Monitoring of twins with twin-to-twin transfusion syndrome.
Fetal Diagn. Ther. 17: suppl. 1, 39-40.
[4] Bruner J.P., Andreson T.L., Rosemond R.L. (1998) Pla-
cental pathophysiology of the twin oligohydramnios-polyhydramnios sequence and the twin-twin transfusion syndrome. Placenta 19: 81-86.
[5] Fisk N.M., Taylor M.J.O. (2001) The fetus(es) with twin
transfusion syndrome. [In:] The unborn patient: the art
and science of fetal therapy. Ed. M.R. Harrison, Phila-
delphia: W.B. Saunders, 315-325.
[6] Gaziano E., Gaziano C., Brandt D. (1998) Doppler veloci-
metry determined redistribution of fetal blood flow: correlation with growth restriction in diamniotic monochorionic and dizygotic twins. Am. J. Obstet. Gynecol. 178:
1359-1367.
[7] Giles W., Trudinger B., Cook C., Connelly A. (1993) Pla-
cental microvascular changes in twin pregnancies with
abnormal umbilical artery waveforms. Obstet. Gynecol.
81: 556-559.
[8] Giles W.B., Trudinger B.J., Cook C.M., Connelly A.J.
(1990) Umbilical artery waveforms in triplet pregnancy.
Obstet. Gynecol. 75: 813-816.
[9] Gosling R.G., Dunbar G., King D.H. et al. (1971) The
quantitative analysis of occlusive peripheral arterial disease by a non-intrusive ultrasonic technique. Angiology 22:
52-55.
[10] Gramellini D., Folli M.C., Raboni S. et al. (1992) Cere-
bral-umbilical Doppler ratio as a predictor of adverse
perinatal outcome. Obstet. Gynecol. 79: 416-420.
[11] Haberman S., Haratz-Rubinstein N., Baxi L., Heller D.
(1997) Power Doppler sonography in monochorionic twins:
a preliminary study. J. Mater. Fetal Investig. 7: 84-88.
[12] Hecher K., Ville Y., Nicolaides K.H. (1995) Fetal arterial
Doppler studies in twin-twin transfusion syndrome. J.
Ultrasound. Med. 14: 101-108.
[13] Hecher K., Ville Y., Snijders R., Nicolaides K. (1995) Dop-
pler studies of the fetal circulation in twin-to-twin transfusion syndrome. Ultrasound. Obstet. Gynecol. 5: 318-324.
[14] Indik J.H., Chen V., Reed K.L. (1991) Association of umbilical venous with inferior vena cava blood flow velocities. Obstet. Gynecol. 77: 551-557.
[15] Jensen O.H. (1993) Doppler velocimetry and umbilical
cord blood gas assessment of twins. Eur. J. Obstet. Gynecol. Reprod. Biol. 49: 155-159.
[16] Malinowski W., Ropacka M. (2003) Zespół przetaczanie
krwi między płodami. [In:] Ciąża wielopłodowa. Ed.
Bręborowicz G.H., Malinowski W., Ronin-Walknowska E.,
Ośrodek Wydawnictw Naukowych, Poznań, 194-222.
[17] Ohno Y., Ando H., Tanamura A. et al. (1994) The value of
Doppler ultrasound in the diagnosis and management of
twin-to-twin transfusion syndrome. Arch. Gynecol. Obstet.
255: 37-42.
[18] Rizzo G., Arduini D., Romanini C. (1994) Cardiac and extracardiac flows in discordant twins. Am. J. Obstet. Gynecol. 170: 1321-1327.
[19] Ropacka M., Markwitz W., Bręborowicz G.H. (2001) Pa-
thophysiology, pathogenesis and diagnosis of transplacental fetofetal transfusion. Arch. Perinat. Med. 7: 13-17.
[20] Ropacka M., Markwitz W., Bręborowicz G.H. (2000) Diagnostyka zespołu transfuzji płodowo-płodowej. Klin. Peri-
nat. Ginek. 30: 40-46.
[21] Ropacka M. (2003) Diagnostyka ultrasonograficzna w ciąży wielopłodowej. [In:] Ciąża wielopłodowa. Ed. Bręborowicz G.H., Malinowski W., Ronin-Walknowska E., Poznań, Ośrodek Wydawnictw Naukowych, 65-85.
[22] Ropacka M., (2003) Ultrasonografia dopplerowska ciąży
wielopłodowej. [In:] Ciąża wielopłodowa. Ed. Bręborowicz
G.H., Malinowski W., Ronin-Walknowska E. Poznań, Ośrodek Wydawnictw Naukowych 87-106.
[23] Suzuki S., Sawa R., Yoneyama Y. et al. (1999) Fetal mid-
dle cerebral artery Doppler waveforms in twin-twin transfusion syndrome. Gynecol. Obstet. Invest. 48: 237-240.
[24] Taylor M.J., Denbow M.L., Duncan K.R. et al. (2000) Antenatal factors at diagnosis that predict outcome in twintwin transfusion syndrome. Am. J. Obstet. Gynecol. 183:
1023-1028.
[25] Taylor M.J., Farquharson D., Cox P.M., Fisk N.M. (2000)
Identification of arterio-venous anastomoses in vivo in monochorionic twin pregnancies: preliminary report. Ultra-
sound Obstet. Gynecol. 16: 218-222.
[26] Trespidi L., Boschetto C., Caravelli E. et al. (1997) Serial
amniocenteses in the management of twin-twin transfusion syndrome: when is it valuable? Fetal Diagn. Ther. 12:
15-20.
[27] Vetter K. (1993) Considerations on growth discordant
twins. J. Perinat. Med. 21: 267-272.
J
MariolaRopacka-Lesiak
Department of Perinatology and Gynecology
Medical University in Poznań
60-535 Poznań, Polna 33, Poland