Human Reproduction vol.14 no.8 pp.2124–2130, 1999
Outcome of twin pregnancies complicated by single
intrauterine death in relation to vascular anatomy of the
monochorionic placenta
Rekha Bajoria1, Ling Y.Wee, Shaheen Anwar and
Stuart Ward
University of Manchester, St Mary’s Hospital, Department of
Obstetrics & Gynaecology, Whitworth Park, Manchester M13 OJH,
UK
1To
whom correspondence ahould be addressed
The objective of this study was to determine the relationship
between the type of placentation, vascular anatomy of the
monochorionic (MC) placenta and the perinatal outcome
of the surviving twin following a single intrauterine fetal
death (IUFD). In this retrospective study, 92 twin pregnancies complicated by a single intrauterine death were identified from three tertiary referral centres [50 MC and 42
dichorionic (DC)]. Antenatal and neonatal data as well as
information on the chorionicity, vascular anastomoses, and
autopsy findings were also obtained. The percentage risk
of IUFD (26 versus 2.4; P < 0.001), anaemia (51.4 versus
0; P < 0.001) and intracranial lesions at birth (46 versus
0; P < 0.001) was greater in MC than in DC twins. In MC
twins without twin–twin transfusion syndrome (TTTS),
perinatal mortality was higher in the group with superficial
arterioarterial (AA)/venovenous (VV) channels than those
with only multiple bidirectional arteriovenous (AV) anastomoses (12/15 versus 0/8; P < 0.001). However, in the TTTS
pregnancies (n J 26), perinatal outcome of the surviving
twin was dependent on whether the recipient (n J 16) or
the donor twin (n 5 10) died first. Incidence of IUFD
(9/16 versus 0/10; P < 0.001), severe anaemia (7/7 versus
1/10; P < 0.001) and intracranial lesions at birth (6/7 versus
2/10; P < 0.001) was common in pregnancies where the
recipient twin died first. In the TTTS group, unidirectional
AV anastomotic channels were found in all but two placentae. In conclusion, this study suggests that the outcome of
twin pregnancies complicated by IUFD is dependent on
the type of vascular anastomoses and TTTS.
Key words: co-twin demise/monochorionic multiple pregnancy/
placental vascular anastomoses/polyhydramnios
Introduction
Antepartum death of a single fetus complicates 2.5–5% of
twin pregnancies and may be associated with a significant
morbidity and mortality in the surviving co-twin (Gaucherand
et al., 1994; Murphy, 1995; Bajoria and Kingdom, 1997). In
monochorionic (MC) pregnancies the perinatal loss rates and
risk of death or neurological handicap in the surviving cotwin is 3–4-fold greater than for dichorionic (DC) pregnancies
2124
(Enbom, 1985; Benirschke, 1993). However, regardless of
the chorionic status, none of these complications occurs in
pregnancy with the vanishing twin (Landy and Keith, 1998).
The precise cause of poor perinatal outcome of the surviving
co-twin in MC pregnancies is unknown. Acute haemodynamic
imbalance resulting from anastomotic flow is considered to be
the likely mechanism (Fusi and Gordon, 1990; Fusi et al.,
1991). Although the chorionic plate vascular anatomy of MC
placenta was first described more than a century ago (Schatz,
1890), no studies to date have made an attempt to relate the
vascular anatomy to the perinatal mortality and morbidity of
the surviving co-twin. Many clinical studies have considered
the presence of superficial vascular anastomoses to be a risk
factor for the surviving twin (Bejar et al., 1990; Fusi et al.,
1991) but have failed to provide comparative data on
anastomoses and favourable outcome. Anecdotal data suggest
that the risk of occurrence of co-twin sequelae is 3-fold greater
in MC pregnancies complicated by twin–twin transfusion
syndrome (TTTS) (Arts et al., 1996). Recently studies have
shown that TTTS is caused by the presence of a unidirectional
deep arteriovenous (AV) shunt with paucity of superficial
anastomoses (Bajoria et al., 1995; Machin et al., 1996; Bajoria,
1998b). Furthermore, it has been suggested that it is the
superficial anastomoses which are responsible for acute transfusional complications following intrauterine fetal death (IUFD)
of one of the twins (Fusi et al., 1991). Taken together, this
evidence raises the possibility that the risk to the surviving
MC co-twin may depend upon the type and the size of the
vascular shunts, rather than the presence or absence of superficial anastomoses.
The aim of this study was to establish if there was an
association between placental vascular anatomy of twin pregnancies complicated by a single intrauterine death and the
perinatal outcome of the surviving co-twin. In addition, in
TTTS pregnancies an attempt was also made to determine the
neonatal outcome of the surviving twin in relation to whether
antepartum death of the donor or the recipient twin occurred
first. This information is important as it may influence the
clinical management of this unusual and difficult problem,
especially since delineation of superficial vascular anastomoses
by power Doppler has now become a realistic possibility
(Fortunato, 1996; Haberman et al., 1997).
Materials and methods
This retrospective study was conducted at Queen Charlotte’s Hospital,
London, UK (1980–1995), Hammersmith Hospital, London, UK
(1980–1997) and St Mary’s Hospital, Manchester, UK (1991–1998).
Twin pregnancies complicated by intrauterine death of one twin were
© European Society of Human Reproduction and Embryology
Co-twin sequelae and vascular anastomoses
identified using a triple system of data collection. Mothers who
underwent abortion, had acardiac twins or who delivered before 20
weeks of gestation were excluded from the study. Twin gestations
complicated by antepartum death were identified from the delivery,
neonatal and perinatal pathology log books. The mother’s antenatal
record, neonatal chart, and neonatal discharge summaries were
reviewed. Autopsy and histology reports were also obtained. Information relating to a range of antenatal, intrapartum and neonatal
complications was also retrieved. The approximate time interval
between the death of the first twin and the delivery of the surviving cotwin was also calculated from information recorded in the case notes.
Information on associated maternal complications such as preeclampsia, diabetes and fetal wellbeing were collected. Ultrasound
scan data particularly in relation to chorionicity, fetal growth, liquor
volume and diagnosis of TTTS were obtained. The diagnosis of
TTTS was made subject to the following criteria: (i) monochorionic
placentation; (ii) discordance in estimated birthweight of .15%; and
(iii) oligohydramnios in the smaller and polyhydramnios in the larger
twin sac. Management details of TTTS pregnancies were also obtained.
Women with TTTS were managed by serial amnioreduction. One
patient who underwent laser ablation of the anastomosing placental
surface vessels was excluded from the study.
Following IUFD, the decision when to deliver the surviving twin
was at the discretion of the consultant in charge. In mothers treated
conservatively, fetal growth and wellbeing were monitored by ultrasound scans, biophysical profiles and Doppler studies. Elective
delivery was only undertaken if there was a risk of fetal compromise,
threatened preterm labour or chorio-amnionitis.
In the surviving twins, neonatal information at birth on haemoglobin, blood transfusion, and cranial ultrasound scan findings were
obtained. The long-term follow-up data in relation to neurological
handicap were obtained from the neonatal notes. In this study, only
information on major neurological handicaps such as cerebral palsy,
blindness and paralysis was obtained.
Autopsy data on twins who died in utero or in the early neonatal
period were also collected in relation to intrauterine growth restriction,
hydrops, pallor, congestion and cardiomegaly. Histological information on the placenta such as chorionicity, marginal (within 1 cm of
placental margin) or velamentous cord insertion, and the type of
vascular anastomotic channels was obtained.
Statistical analysis
All results were expressed as median and range. Two groups were
compared by the Mann–Whitney test for continuous variables and by
Fisher’s exact test for blocked variables.
Results
During the study period, 101 twin pregnancies complicated by
a single IUFD were identified. Four monoamniotic and five
diamniotic (DA) pregnancies were excluded because information on the type of anastomoses and/or neonatal data were
not available. Perinatal outcome data on 92 twin pregnancies
in relation to chorionicity, TTTS and type of vascular anastomoses are reported.
Comparison between MC and DC twin pregnancies (Table I)
The median gestational age of first intrauterine death in MC
pregnancies (n 5 50) was comparable to that of DC pregnancies. However, the median gestational age at delivery of the
second twin in MC was lower than in DC twins (P , 0.002).
In MC twins, incidence of IUFD of the co-twin (13/50 versus
1/42; P , 0.001), and total perinatal mortality rate (29/50
versus 9/42; P , 0.01) were higher than DC twins. In the MC
group, anaemia was found in 19/37 of the surviving co-twins
while polycythaemia with a haematocrit of 95 was present in
only one twin. In contrast, none of the surviving co-twins in
the DC group required blood transfusion. Prior to intrauterine
demise of the first twin, discordance in estimated birthweight
was more common in MC than DC twins (39/50 versus 13/42;
P , 0.01).
Comparison in MCDA twins with or without TTTS (Tables
II and III)
When the outcomes of pregnancies in MC twins were analysed
in relation to TTTS, the median (range) gestational age of
death of one twin was greater in non-TTTS than TTTS
pregnancies [28.5 (21.5–38) versus 25.2 (22.3–34) weeks; P ,
0.0001]. Similar differences were also found in gestational age
at delivery [30 (21.6–38) versus 27.1 (22.3–35) weeks; P ,
0.009]. Incidence of intrauterine death of the second twin
(4/24 versus 9/26), and total perinatal mortality (12/24 versus
17/26) were similar in the two groups. Similarly, the incidence
of anaemia (11/20 versus 8/17), significant abnormality on the
intracranial scan (15/20 versus 14/17) were not significantly
different between the two groups. Histology confirmed MCDA
placentation. In the non-TTTS group (Table II), 15 placentae
had superficial anastomoses of arterioarterial (AA)/venovenous
(VV) type, whereas nine had only multiple deep arteriovenous
(AV)/venoarterial (VA) anastomoses. In contrast, 24 placentae
with TTTS had only deep AV anastomoses, whereas additional
superficial anastomoses were found in only two placentae. The
frequency of abnormal cord insertion between the two groups
was comparable. Individual data of both the groups are given
in Tables II and III.
In the non-TTTS pregnancies, incidence of intrauterine death
(4/15 versus 0/9; not significant), and among live births,
incidence of anaemia (10/11 versus 1/9; P , 0.05), intracranial
lesions (9/11 versus 2/9; P , 0.01) and neurological handicap
in the surviving co-twin (i.e. excluding IUFD and neonatal
death 2/3 versus 0/9; P , 0.05) were more common in the
presence of superficial placental anastomoses compared with
multiple AV/VA anastomoses.
TTTS pregnancies in relation to demise of the recipient or
donor twin (Table III)
In 26 cases of pregnancies complicated by chronic midtrimester TTTS, data sets were divided into two subsets
according to whether the recipient or the donor twin died first.
In 16 women, the recipient twin died first while in 10 cases,
donor twin death occurred first.
The median (range) gestational age of intrauterine death of
the first twin was comparable between the two groups [25
(22.3–34) versus 28.4 (23–30) weeks]. The median gestational
age at delivery in the group where the donor twin died first
was greater than those pregnancies where the recipient twin
died first [29.3 (26.2–34.2) versus 25 (22.3–34.1); P , 0.004].
Similarly, intrauterine death (9/16 versus 0/10; P , 0.001),
and total perinatal mortality rate (15/16 versus 2/10; P ,
0.001) were higher with first death of the recipient than the
2125
R.Bajoria et al.
Table I. Outcome of the surviving co-twin in relation to chorionicity
Parameters
Monochorionic twins
(n 5 50)
Dichorionic twins
(n 5 42)
P value
Gestational age at first IUFD (weeks)a
Gestational age at delivery (weeks)a
Interval between IUFD and delivery (days)a
Outcome of co-twins
1. IUFD (n)
2. Alive at birth (n)
3. Neonatal death (n)
4. Anaemia at birth
Hb at birth (g/dl)a
Blood transfusion (n)
Polycythaemia at birth (n)
5. Abnormal cranial ultrasound scanb
Neurological handicapc
Autopsy (n)
1. Twin–twin transfusion syndrome
2. IUGR
First IUFD
Second IUFD
3. Hydrops
First IUFD
Second IUFD
Placenta
Abnormal cord insertion (n)
1. First death
2. Co-twin
28 (21.5–38)
28.8 (21.6–38)
2 (0.02–84)
29.5 (14–39)
33.2 (24–40.3)
1.6 (0.08–185)
NS
0.002
NS
13
37
16
19
10.5 (6.7–13.5)
19
1 (Ht 5 95)
17
2
1
41
8
None
0.001
NS
0.01
0.001
None
0.001
None
0
0.001
NS
26
0
0.001
24
9
12
1
0.03
0.013
16
0
MCDA
0
0
DCDA
0.001
NS
32
30
9
8
0.001
0.001
aValues are
bExcluding
medians with ranges in parentheses.
transient echo-dense area.
major neurological handicaps were scored, including cerebral palsy, blindness and paralysis in the surviving twins.
IUFD 5 intrauterine fetal death; NS 5 not significant; Ht 5 haematocrit; IUGR 5 intrauterine growth retardation; MCDA 5 monochorionic–diamniotic;
DCDA 5 dichorionic–diamniotic.
cOnly
donor twin. Frequency of anaemia requiring blood transfusion
was also higher in the group where the recipient twin died
first (excluding IUFD) than when death of the donor twin
occurred first (7/7 versus 1/10; P , 0.001). Examination of
the placenta confirmed monochorionicity. The frequency of
abnormal cord insertion was comparable between two groups.
The chorionic plate vascular anatomy between the groups was
comparable in terms of presence of AV anastomoses with or
without superficial AA/VV shunts. Intrauterine demise of
the donor was associated with spontaneous resolution of
polyhydramnios and hydrops in 6/10 recipient twins. The
perinatal outcome in relation to vascular anatomy is summarized in Figure 1.
Discussion
This study shows that the perinatal outcome of a surviving
twin depends upon the type of placentation and confirms the
notion that the risk of neurological handicap/death in the cotwin is greater in MC than DC pregnancies (Murphy, 1995).
Although in the majority of cases the cause of the first
intrauterine death remained indeterminate, discordant fetal
growth, polyhdramnios–oligohydramnios, and abnormal cord
insertion were more common in MC than DC twins.
Traditionally, it has been believed that the demise/neurological lesion of the co-twin is due to the passage of thrombotic
or necrotic materials from the dead to the healthy twin along
placental vascular shunts (Benirschke, 1993). The validity of
this idea has been questioned recently because of the normal
2126
coagulation status and anaemia in the survivors (Okamura
et al., 1994). The data reported in this study provide a
morphological basis to the haemodynamic imbalance theory
which states that placental anastomoses allow transfer of blood
from the surviving twin to the dead co-twin, giving rise to
periods of hypoperfusion resulting in neurological changes
(Bajoria and Kingdom, 1997). Therefore, transfusion of biologically active compounds from the dead to the surviving
twin is unlikely.
We found a normal outcome in the surviving recipient twin
following the sudden demise of the donor twin. All except
one recipient twin had a normal haemoglobin at birth with
no adverse neurological outcome. Furthermore, resolution of
polyhydramnios and hydrops in the majority of the recipient
twins suggests that neither the transfusion of blood nor the
passage of acute thrombotic material between the fetuses took
place. This favourable outcome can be explained on the basis
of the type of the anastomotic channels present in the fetoplacental unit. All except one placenta had AV anastomoses
connecting the arterial circulation of the donor to the venous
end of the recipient twin. It has previously been shown,
using controlled perfusion experiments, that AV shunts allow
unidirectional flow, i.e. from the artery to vein (Bajoria et al.,
1995; Bajoria, 1998a,b). It is therefore conceivable that a
favourable outcome for the recipient twin might be attributed
to no flow between the surviving and dead twins simply
because of the negative pressure gradient along the AV
anastomoses (dead donor with zero and alive recipient twin
with higher systemic pressure).
Birth
weight
of first
IUFD (g)
M/M
M/M
F/F
F/F
F/F
M/M
M/M
F/F
M/M
F/F
F/F
5
6
7
8
9
10
11
12
13
14
15
880
1300
1325
980
210
2785
380
310
1383
310
620
670
1160
1390
1850
1260
1320
1012
420
2745
2600
880
1344
480
1450
850
1140
1284
1160
Birth
weight of
co-twin
(g)
M/M
F/F
M/M
M/M
M/M
F/F
F/F
F/F
2
3
4
5
6
7
8
9
2240
833
920
940
880
2260
1540
577
2940
3264
2470
1200
2108
1850
2060
1820
1160
1940
38
30
28.3
35
31
34
31
24
37
28.4
31.4
30
28.5
21.5
35.3
28.2
27.1
28
24.4
30.1
28.1
27
28.3
27.1
Gestational
age at first
death
(weeks)
38
38
29
36
31
34.3
32
27.5
38
30.2
32
30
29
21.6
35.4
35
27.3
28
24.4
30.1
28.4
27
28.3
27.1
Gestational
age at
delivery
(weeks)
days
days
h
h
Marginal
Vel
Marginal
Central
Vel
Marginal
Central
Marginal
Vel
Vel
Central
Marginal
Central
Marginal
Central
Central
Marginal
Marginal
Vel
Vel
Marginal
Central
Marginal
Central
Cord
insertion
first
death
and live birth of the co-twin.
2h
56 days
4 days
7 days
12 h
3 days
7 days
26 days
7 days
12 days
3 days
1 days
2 days
1 day
1 day
47
2
8
3
12 h
3 days
4–6 h
1 day
1 day
Time
interval
(h/days)a
Marginal
Vel
Vel
Vel
Marginal
Central
Marginal
Marginal
Central
Marginal
Central
Vel
marginal
Central
Marginal
Central
Marginal
Marginal
Marginal
Central
Marginal
Central
Marginal
Marginal
Cord
insertion
co-twin
MultipleMultipleMultipleSeveral
AV/VA
Multiple
AV,VA
Multiple
Bi-direction
Multiple
Multiple
Several
AA
AA/VV
AA/VV
VV, AV
AA
VV/AA
AA, VV
AA, VV
VV, AA
VV/AA
AA
AA
AA,
AA
AA
Type of
shunts
15.5
N/A
15.9
15
16.5
No
No
No
No
No
Yes
95b
16.8
14.8
Yes
area
No
No
Yes
No
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Blood
transfusion
12.5
11.5
14.5
8.9
9.8
11.2
10.5
12.5
10.7
6.7
7.6
8.5
Hb
(g/dl)
IVH
Echo-dense
area
Echo-dense
area
N/A
IVH
N/A
Echo-dense
area
N/A
Echo-dense
Echo-dense
area
IVH, PVL
IVH
IVH, PVL
IVH
N/A
IVH, PVL
IVH
IVH
Cyst
IVH
Cranial
scan
findings
NGA
MSB
MSB
MSB
NGA
NGA, pale
MSB
MSB
NGA
IUGR,
congested/
pale
NGA
NGA/NA
Congested/
Congested/
pale
Congested/
pale
NGB/NGB
MSB/pale
IUGR/
congested
MSB
Congested/
pale, NGA
MSB/NA
MSB/pale
Congested/
pale
NGA
Autopsy
findings
Alived
Alived
Well
Well
Well
Well
Well
Well
Alived
NND
(1 day)
Well
IUFD
IUFD
IUFD
IUFD
Alive, Cerebral
palsy, blindness
Alive, spastic
NND (4 days)
NND (31 h)
NND (20 h)
NND (3 days)
NND (2 days)
NND (4 days)
NND (23 h)
Outcome
(time after
birth)
dLost to follow-up.
M 5 male; F 5 female; AA 5 arterioarterial; VV 5 venovenous; AV 5 arteriovenous; VA 5 venoarterial; Vel 5 velamentous cord insertion; MSB 5 macerated still birth; NGA 5 no gross abnormality;
Gest 5 gestation; Hb 5 haemoglobin; NND 5 neonatal death; IUFD 5 intrauterine fetal death; IUGR 5 intrauterine growth retardation; IVH 5 intraventricular haemorrhage; NA 5 not applicable; N/A 5
not available; PVL 5 periventricular leukomalacia; Vel 5 velamentous.
aTime interval between first and second death and/or between first death
bHaematocrit.
cMultiple AV/VA anastomoses 5 deep bi-directional anastomoses only.
F/F
1
With multiple AV/VA anastomosesc
M/M
F/F
F/F
2
3
4
With superficial AA/VV
1 F/F
1148
Sex
Table II. Perinatal outcome of co-twins after a single fetal death in 24 monochorionic twin pregnancies without twin–twin transfusion syndrome
Co-twin sequelae and vascular anastomoses
2127
2128
Birth
weight
of first
IUFD (g)
F/F
M/M
F/F
M/M
M/M
F/F
M/M
F/F
F/F
M/M
F/F
F/F
death donor
M/M
1272
F/F
710
F/F
500
F/F
M/M
M/M
F/F
F/F
M/M
F/F
5
6
7
8
9
10
11
12
13
14
15
16
First
1b
2b
3
4b
5
6b
7
8
9
10
1567
1015
736
2820
1600
1290
1059
1600
1192
1870
1143
400
470
1925
480
458
420
480
560
698
420
690
750
590
1670
920
Birth
weight of
co-twin
(g)
For abbreviations see Table II.
30.2
29.5
26.2
35
31.6
28
29
29
28.6
34.2
30.2
23.5
25
34.1
25
23.4
24.4
22.3
25.1
24.2
26
25.1
28
25
33.2
28
Gestational
age at
delivery
(weeks)
2
24
5
84
21
3
28
days
days
days
days
days
days
days
6h
4 days
39 days
2 days
2 days
12 h
1 days
2h
2 days
12 h
16 h
2 days
8h
6h
12 h
10–12 h
8–10 h
0.5 h
12 h
Time
interval
(h/days)a
Marginal
Marginal
Vel
Marginal
Marginal
Central
Marginal
Vel
Marginal
Vel
Central
Marginal
Vel
Marginal
Vel
Marginal
Marginal
Marginal
Marginal
Marginal
Central
Central
Central
Marginal
Marginal
Marginal
Cord
insertion
first
death
and/or between first death and live birth of the co-twin.
30
26.2
25.4
23
28.6
27.4
25
29
28.2
28.5
30
23.3
25
34
25
22.4
24.2
22.3
24.6
24
26
25
27.6
25
33.2
28
Gestational
age at first
death
(weeks)
aTime interval between first and second death
bRecipient twins were hydropic at birth.
847
232
444
250
1258
540
570
1251
650
580
2430
600
632
640
525
609
846
760
810
1050
F/F
4
720
2205
M/M
M/M
2
3
First death recipient
M/M
1200
Sex
Marginal
Marginal
Marginal
Marginal
Central
Central
Vel
Marginal
Marginal
Marginal
Vel
Marginal
Central
Central
Central
Marginal
Central
Central
Marginal
Central
Marginal
Central
Marginal
Marginal
Marginal
Marginal
Cord
insertion
co-twin
AV
AV
AV
AV
2 AV
AV
AV
VV
AV
AV
AA, AV
AV
AV
3 AV
AV
AV
AV
AV
AV
AV
AV
AV
AV
AV
AV
AV
Type of
shunts
14.8
17.1
16.1
15
16.8
16
15.2
7.6
16.4
15.5
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
13.5
N/A
10.2
10.8
11.7
9.7
12.5
8.7
Hb
(g/dl)
/Ht
no
no
no
no
no
No
no
Yes
no
no
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
Yes
N/A
Yes
Yes
Yes
Yes
Yes
Yes
Blood
transfusion
Table III. Perinatal outcome of co-twins after a single fetal death in 26 monochorionic twin pregnancies without twin–twin transfusion syndrome
IVH
Echo-dense
Porencephalic cyst
Echo-dense
N/A
Flare
N/A
Flare
Echo-dense
Echo-dense
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
IVH, cyst
N/A
IVH
IVH, PVL
cyst
N/A
IVH
Echo-dense
IVH, cyst
Cranial
scan
findings
IUGR
MSB
MSB
MSB
MSB
MSB
MSB
IUGR/NA
MSB
MSB
Hydropic
congested/IUGR
Hydropic,/IUGR
Hydropic
congested
Hydropic
congested/IUGR
Hydropic,
congested/pale,
IUGR
Hydropic,
lethoric/IUGR
Hydropic/IUGR
Plethoric,
hydropic/IUGR,
pale
N/A
Hydropic,
congested/IUFD
Hydropic,
congested/IUGR,
pale
Hydropic,
congested/IUGR,
pale
Hydropic/
IUGR, pale
Hydropic,
congested/IUGR,
pale
Hydropic/IUGR,
pale
Hydropic/
Autopsy
findings
NND (7 h)
Alive, well
Well, no
handicap
Well
Alive, well
NND (7 days)
Well
Alive
alive
Alive
IUFD IUGR,
pale
IUFD
IUFD
IUFD
IUFD
IUFD
IUFD
UGR
NND (2 days)
IUFD
NND (23 h)
NND (2 days)
NND (2 days)
NND (5 days)
Alive, well
NND (5 days)
Outcome
(time after
birth)
R.Bajoria et al.
Co-twin sequelae and vascular anastomoses
Figure 1. Illustration of the perinatal outcome of twin pregnancies
complicated by a single intrauterine death in relation to vascular
anatomy of the placenta.
In keeping with this proposition, data from this study also
show that in placentae with unidirectional AV anastomoses,
death of the recipient twin was invariably associated with
intrauterine or neonatal death of the donor twin. As all the
seven donor twins born alive were severely anaemic and
required blood transfusion, transfer of blood along the unidirectional anastomoses seems to be the most likely explanation
for such a dismal outcome in this group. The direction of
the blood flow through AV anastomoses argues against the
possibility of transfer of thrombotic material from the dead to
the live donor twin. Furthermore, formation of thrombotic
material is unlikely because of the temporal proximity of the
sequelae to the initial recipient twin death (~48 h). Consistent
with this proposition, autopsy finding on twin pairs dying
in utero revealed pallor in the donor and polycythaemia in the
recipient twin.
Hence, from the clinical perspective, these data suggest that
in the event of intrauterine demise of the recipient twin, the
donor can only be rescued by prompt delivery after 28 weeks
gestation. However, in pregnancies where both twins are still
viable, an alternative option such as the occlusion of the
umbilical cord of the recipient twin is a distinct possibility
(Bebbington et al., 1995; Deprest et al., 1996).
We also observed a higher incidence of co-twin sequelae
in terms of intrauterine death, neonatal anaemia, abnormal
intracranial ultrasound scan, and neurological handicap in the
presence of superficial AA/VV anastomoses. In our cohort
only one of the placentae had VV anastomoses in isolation.
The severity of anaemia and the autopsy findings from twin
pairs who died in utero further lend credence to the haemodynamic theory. It is conceivable that in the presence of
superficial AA anastomoses, a massive transfer of blood can
occur, against the pressure gradient from the live to the dead
twin. This may cause brain damage or fetal demise of the
surviving twin simply because of severe haemodynamic
imbalance. However, transfusion of thrombotic material from
the dead to the live fetus is virtually impossible because the
pressure gradient is such that flow from the dead to the live
fetus cannot take place.
A favourable neonatal outcome was seen in MC pregnancies
with multiple bidirectional AV anastomoses without superficial
anastomoses. None of the twins in this category had significant
anaemia at birth and had normal neurodevelopment. On the
other hand, one baby who was born alive had severe polycythaemia (haematocrit of 94) and required an exchange
transfusion. The optimal outcome of MC twins can only be
explained on the basis of attainment of a dynamic steady state
along the AV and VA anastomotic channels with oppositely
directed anastomotic blood flow. We speculate that in this
group, following the demise of one twin, a massive blood
transfusion must have occurred from the survivor’s arterial to
the dead twin’s venous circulation (AV). In the dead twin, this
may lead to a rise in the systemic filling pressure which then
in turn can initiate the flow along the VA anastomoses with
the establishment of an intertwin circulation. In this cohort, it
is theoretically possible that thrombotic material generated in
the dead twin may reach the circulation of the viable fetus.
However, the normal outcome in eight cases with no evidence
of neurological handicap argues against the thromboembolic
episode as the cause for co-twin sequelae.
The retrospective nature of this study means that information
relating to the vascular anastomoses may be incomplete. We
accept that delineation of vascular shunts by conventional
techniques may not be as accurate and precise as reported
previously where controlled perfusion experiments were undertaken (Bajoria, 1998b). Nevertheless, identification of superficial channels by injection technique is quite simple and does
not require a high degree of skill. Furthermore, in this study
we evaluated, in the first instance, the data according to the
presence or absence of superficial anastomoses. Only in the
group without superficial anastomoses were direction and
numbers of AV anastomoses taken into account. The data
relating to TTTS placentae generated by a conventional injection method in this study agrees, at least in principle, with the
previously published data where physiological techniques were
used (Bajoria et al., 1995; Bajoria, 1998a,b). Furthermore, the
primary objectives of this study were to evaluate the relationship between the co-twin sequelae and the type of shunt.
Further prospective study is necessary to confirm these findings.
In conclusion, our data suggest that the co-twin sequelae
are dependent upon the type of chorionic plate vascular
2129
R.Bajoria et al.
anatomy. Development of newer techniques to map the vascular
anatomy of MC placentae accurately in vivo are therefore
warranted as the availability of such information during the
antenatal period is likely to influence the clinical management
and prevent neurological handicap in at least some of the
surviving co-twins.
Acknowledgements
We are grateful to the staff of Perinatal Pathology, Centre of Fetal
Care, Labour Ward and Neonatal Unit of Queen Charlotte’s and
Hammersmith Hospital for their assistance in the collection of the
clinical data.
References
Arts, H., van Eyck, J. and Arabin, B. (1996) Fetal death of one twin in a
monochorionic pregnancy with twin–twin transfusion syndrome. J. Reprod.
Med., 41, 775–778.
Bajoria, R. (1998a) Abundant vascular anastomoses in monoamniotic versus
diamniotic monochorionic placentas. Am. J. Obstet. Gynecol., 179, 788–793.
Bajoria, R. (1998b) Vascular anatomy of monochorionic placenta in relation
to discordant growth and amniotic fluid volume. Hum. Reprod., 13,
2933–2940.
Bajoria, R. and Kingdom, J. (1997) A case for routine determination of
chorionicity and zygosity in multiple pregnancies. Prenat. Diagn., 17,
1207–1225.
Bajoria, R., Wigglesworth, J. and Fisk, N.M. (1995) Angioarchitecture of
monochorionic placentas in relation to the twin–twin transfusion syndrome.
Am. J. Obstet. Gynecol., 172, 856–863.
Bebbington, M.W., Wilson, R.D. Machan, L. and Wittmann, B.K. (1995)
Selective feticide in twin transfusion syndrome using ultrasound-guided
insertion of thrombogenic coils. Fetal Diagn. Ther., 10, 32–36.
Bejar, R., Vigliocco, G., Gramajo, H. et al. (1990) Antenatal origin of
neurologic damage in newborn infants. II. Multiple gestations. Am. J.
Obstet. Gynecol., 162, 1230–236.
Benirschke, K. (1993) Intrauterine death of a twin: mechanisms, implications
for surviving twin, and placental pathology. Semin. Diagn. Pathol., 10,
222–231.
Deprest, J.A., Evrard, V.A., Van Schoubroeck, D. and Vandenberghe, K.
(1996) Endoscopic cord ligation in selective feticide. [Letter.] Lancet, 348,
890–891.
Enbom, J.A. (1985) Twin pregnancy with intrauterine death of one twin. Am.
J. Obstet. Gynecol., 152, 424–429.
Fortunato, S.J. (1996) The use of power Doppler and color power angiography
in fetal imaging. Am. J. Obstet. Gynecol., 174, 1828–1833.
Fusi, L. and Gordon, H. (1990) Twin pregnancy complicated by single
intrauterine death. Problems and outcome with conservative management.
Br. J. Obstet. Gynaecol., 97, 511–516.
Fusi, L., McParland, P., Fisk, N. et al. (1991) Acute twin–twin transfusion: a
possible mechanism for brain-damaged survivors after intrauterine death of
a monochorionic twin. Obstet. Gynecol., 78, 517–520.
Gaucherand, P., Rudigoz, R.C. and Piacenza, J.M. (1994) Monofetal death in
multiple pregnancies: risks for the co-twin, risk factors and obstetrical
management. Eur. J. Obstet. Gynecol. Reprod. Biol., 55, 111–115.
Haberman, S., Haratz-ubinstein, N., Baxi, L. and Helle, D. (1997) Power
Doppler sonography in monochoionic twins: a preliminary study. J. Matern.
Fetal Invest., 7, 84–88.
Landy, H.J. and Keith, L.G. (1998) The vanishing twin: a review. Hum.
Reprod. Update, 4, 000–000.
Machin, G., Still, K. and Lalani, T. (1996 Correlations of placental vascular
anatomy and clinical outcomes in 69 monochorionic twin pregnancies. Am.
J. Med. Genet., 61, 229–236.
Murphy, K.W. (1995) Intrauterine death in a twin: implications for the survivor.
In Ward, R.H. and Whittle, M. (eds), Multiple Pregnancy. RCOG Press,
London, pp. 218–31.
Okamura, K., Murotsuki, J., Tanigawara, S. et al. (1994) Funipuncture for
evaluation of hematologic and coagulation indices in the surviving twin
following co-twin’s death. Obstet. Gynecol., 83, 975–978.
2130
Schatz, F. (1890) Die Gefässverbindungen der Placentarkreisläufe eineiiger
Zwillinge, ihre Entwicklung und ihre Folgen. Arch. Gynäkol., 27, 1–72.
Received on February 2, 1999; accepted on April 29, 1999