DOI: 10.1111/j.1471-0528.2006.01027.

Systematic review

www.blackwellpublishing.com/bjog

Prognosis for the co-twin following single-twin

death: a systematic review
SSC Ong,a J Zamora,b KS Khan,c MD Kilbyc
a Department of Fetal Medicine, Birmingham Womens Hospital, Edgbaston, Birmingham, UK b Clinical Biostatistics Unit, Hospital Ramon y Cajal,
Madrid, Spain c Division of Reproduction & Child Health, Birmingham Womens Hospital, Edgbaston, Birmingham, UK
Correspondence: Dr SSC Ong, Department of Fetal Medicine, Birmingham Womens Hospital, Edgbaston, Birmingham B15 2TG, UK.
Email Stephen.ong@btinternet.com

Accepted 9 June 2006. Published OnlineEarly 14 August 2006.

Background Following single-twin death, the perinatal mortality

Main results The search strategy yielded 632 potentially relevant

and morbidity for the surviving co-twin is increased but difficult

to quantify. We present data on prognosis from a systematic
review.

citations. Full manuscripts were retrieved for 54 citations and 28

studies were finally included in the review. Following the death of
one twin, the risk of monochorionic and dichorionic co-twin
demise was 12% (95% CI 711) and 4% (95% CI 27),
respectively. The risk of neurological abnormality in the surviving
monochorionic and dichorionic co-twin was 18% (95% CI 1126)
and 1% (95% CI 07), respectively. The risk of preterm delivery
was 68% (95% CI 5678) and 57% (95% CI 3477), respectively.
Where there was comparative data within studies, the odds of
monochorionic co-twin intrauterine death was six times that of
dichorionic twins (OR 6.04 [95% CI 1.8419.87]). Neurological
abnormality was also higher in monochorionic compared with
dichorionic pregnancies (OR 4.07 [95% CI 1.3212.51]).

Objectives We aimed to determine the incidence of a) co-twin death,

b) neurological abnormality and c) preterm delivery for the surviving

co-twin following single-twin death after 14 weeks of gestation.
Search strategy Literature was identified by searching two

bibliographical databases and specialist journals between

1990 and 2005.
Selection criteria The selected studies of 5 cases reported on

perinatal death and/or neurodevelopmental delay of the

surviving co-twin.
Data collection and analysis Studies were assessed for quality and

data extracted to allow computation of rates. The data were

inspected for heterogeneity using a Forrest plot and examined
statistically using the chi-square test. Data from individual studies
were pooled within subgroups defined by prognosis.

Authors conclusions More prospective research is required to

inform decision making on this subject, especially with data that

allow stratification based upon chorionicity.
Keywords Co-twin demise, prognosis, single-twin demise, twin.

Please cite this paper as: Ong S, Zamora J, Khan K, Kilby M. Prognosis for the co-twin following single-twin death: a systematic review. BJOG 2006;113:
992998.

Introduction
Intrauterine death of one fetus in a twin pregnancy is uncommon in the second or third trimester. However, the consequences to the surviving co-twin can be profound, especially in
monochorionic twins. These may include co-twin death, survival with cerebral impairment or preterm labour with its
sequelae.1 Recent changes in technology and prenatal ultrasound scan have meant that clinicians can diagnose this condition and have the option to intervene. Decision making
should be informed by existing prognostic evidence, but individual studies including data from case reports, follow up of
cohorts and twin registries tend to have imprecise results as the
event is uncommon. More precise information may be

992

obtained by pooling these results statistically in a meta-analysis.

A comprehensive systematic review is required to capture the
literature scattered across many journals. Thus far, existing
reviews2,3 have not been systematic and this may be because
the methodology of meta-analysis involving observational studies is not widely disseminated. We conducted such a review to
provide a reliable estimate of prognosis for the co-twin following single-twin death after the first trimester of pregnancy.

Methods
The project was based on a prospective protocol developed
using widely recommended methods for systematic review of
observational studies.4,5

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology

Prognosis following single-twin death

Sources and study selection

Literature was identified by searching the bibliographic
databases MEDLINE and EMBASE between 1990 and 2005
inclusive. The search term combination captured citations
with the relevant population (e.g. single-twin death; surviving twin) using a combination of MeSH and text words. A
hand search of relevant literature was also conducted from
specialist journals. There was no language restriction in
search or selection.
Our study selection criteria were:
Population: Twin pregnancies with death of one twin.
Outcome: Perinatal death and/or neurodevelopmental
delay of the surviving twin.
Study design: Series with follow up of 5 cases of twin
pregnancies with death of one twin.
From the electronic searches, full manuscripts of all the
potentially relevant citations were obtained. The final inclusion/exclusion decisions were made after evaluation of these
by two reviewers (S.O. and M.K.). In cases of data duplication
(i.e. the same data published in two or more reports), only the
most recent and complete report was included.
We followed a deliberate policy of excluding studies of twin
pregnancies in which a disappearing sac was suspected in the
first trimester of pregnancy.

extracted to allow computation of rates, stratifying by chorionicity and other prognostic factors wherever possible.

Data synthesis
The extracted data were tabulated to allow qualitative inspection for clinical and methodological heterogeneity. Heterogeneity of rates was explored graphically using Forrest plot and
examined statistically using the chi-square test.7 Data from
individual studies were pooled within subgroups defined by
prognosis and outcome.8

Results
Identification of the literature
The electronic search yielded a total of 632 citations, of which
54 were considered potentially relevant. Examination of the
full manuscripts revealed that 26 did not meet the selection
criteria. This was mostly because the case series reported less
than five cases. Thus, a total of 28 primary studies were
selected for review1,2,934 (Figure 1, Table 1). One study was
derived from data obtained from three separate institutions.12
All other studies published data either from follow up of case
series (cohort studies) or from registries.

Quality assessment and data extraction

Study characteristics and quality

One reviewer (S.O.) extracted data from all articles meeting

the selection criteria including data on features of methodological quality. This was double checked by another reviewer
(M.K.). The studies were assessed for quality by the following
criteria derived from existing check-lists:6
Data collection: Prospective collection of data was considered
ideal, retrospective collection was considered second best.
Description of population: A well-defined sample at a uniform early stage with clear documentation of chorionicity
and gestational age of single-twin death was considered ideal.
Prognostic factors considered: Clear documentation of
consideration of prognostic co-factors, including chorionicity, gestation of single-twin death, presence of twintwin
transfusion syndrome, discordant congenital anomalies
and concurrent maternal illness, was considered ideal.
Length of follow up: Follow up beyond 4 weeks following
delivery was considered ideal.
Objective outcome: Outcomes including co-twin death and
validated measures of neurological abnormality of co-twin
survivors were considered ideal.
Outcome ascertainment: Greater than 90% follow up of the
original study population was considered ideal, less than
90% was considered second best.
Data extraction sought information regarding co-twin
intrauterine (or neonatal) death, neurological abnormality
by 4 weeks following delivery in co-twin survivors and preterm delivery before 34 weeks of gestation. Data were

Study characteristics and population are shown in Table 1.

Data from birth registries were extractable for in utero death
of the co-twin but not for neurological abnormality or preterm delivery. Quality of studies summarised in Figure 2
showed that data collection was retrospective in all studies;
chorionicity and gestational age of single-twin death was
reported in 82% (23/28) and 64% (18/28) of studies, respectively; and presence or absence of twintwin transfusion syndrome, discordant congenital anomalies and concurrent
maternal illness was reported in 46% (13/28), 54% (15/28)
and 33% (9/28) of studies, respectively.

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology

993

The risk of co-twin death in utero

Preliminary analysis to assess the risk of co-twin death
involved 20 studies (4503 twin pregnancies). The preliminary
analysis was highly heterogeneous (P = 0.00) for dichorionic
twins, with the heterogeneity contributed by a single study.
This study by Johnson and Zhang14 involved data from a birth
register of unlike-sex twins. In order to compute numbers of
co-twin death, we had to convert percentages to numbers
without the benefit of the availability of raw data. Analysis
revealed that this study contributed to more than one-quarter
of heterogeneity (I2 = 96.5% decreasing to I2 = 71.6% after
exclusion of this study). Accordingly, we excluded the data
from Johnson and Zhang.14
In the final analysis, to assess the risk of co-twin death, data
were derived from 19 studies (904 twin pregnancies) (Figure 3).

Ong et al.

Potentially relevant citations identified by search strategy for Medline

and Embase and hand search (19902005)
n = 632

Citations excluded.
Did not meet selection criteria
n = 578

Citations retrieved for detailed

evaluation of full manuscript
n = 54

Studies excluded.
Did not meet selection criteria
n = 26

Studies included in systematic review

n = 28

Outcome:
in utero death

Outcome:
neurological
abnormality

Outcome:
preterm delivery

n = 19
(904 pregnancies)

n = 17
(267 pregnancies)

n = 11
(100 pregnancies)

Figure 1. Flow diagram of study selection for systematic review. Outcome of surviving co-twin following single-twin death after 14 weeks of gestation.

The risk of monochorionic and dichorionic co-twin death

was 12% (95% CI 718) (heterogeneity P = 0.02) and 4%
(95% CI 27) (heterogeneity P = 0.74), respectively. Where
there was comparative data within studies, the odds of
monochorionic twin death following single-twin death after
20 weeks of gestation was six times higher compared with
dichorionic twins (five studies; OR 6.04 [95% CI 1.84
19.87]; heterogeneity P = 0.56) (Figure 4).

within studies, the odds of neurological abnormality in

monochorionic survivors following single-twin death after
20 weeks of gestation was four times higher compared with
dichorionic survivors (eight studies; OR 4.07 [95% CI 1.32
12.51]; heterogeneity P = 1.00) (Figure 4).

Preterm delivery

To assess the risk of neurological abnormality, data were

derived from 17 studies (267 twin pregnancies) (Figure 3).
The risk of neurological abnormality in the surviving monochorionic and dichorionic co-twin was 18% (95% CI 1126)
(heterogeneity P = 0.45) and 1% (95% CI 07) (heterogeneity
P = 0.81), respectively. Where there was comparative data

To assess the risk of preterm delivery, data were derived from

11 studies (100 twin pregnancies) (Figure 3). The risk of preterm delivery in monochorionic and dichorionic pregnancies
was 68% (95% CI 5678) (heterogeneity P = 0.52) and 57%
(95% CI 3477) (heterogeneity P = 0.40), respectively. These
figures for preterm delivery include both iatrogenic and spontaneous preterm delivery. Preterm delivery before 34 weeks of
gestation appeared to be marginally higher in monochorionic
pregnancies compared with dichorionic pregnancies although

994

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology

The risk of neurological sequelae

Prognosis following single-twin death

Table 1. Studies selected for systematic review and availability of

data for extraction and analysis
Author

Number of
cases

Data extractable
In utero Neurological Preterm
death abnormality delivery

Case series
Abdal-Khalig and
Sobande33
Aslan et al.11
Axt et al.10
Eglowstein and
DAlton30
Fusi and Gordon21
Gaucherand
et al.26
Ishimatsu et al.32
Jou et al.29
Kilby et al.15
Malinowski
et al.23
Malinowski
et al.9
Lin et al.24
Liu et al.34
Petersen and
Nyholm16
Prompeler et al.17
Saito et al.18
Santema et al.19
Sonneveld and
Correy31
van Heteren
et al.20
Wang et al.25
Woo et al.2
Zorlu et al.22
Birth register
Rydhstrom and
Ingemarsson
(1993)27
Rydhstrom (1994)28
Pharoah and Adi1
Glinianaia et al.13
Johnson and
Zhang14
Other
Bajoria et al.12

35

25
7
20

N
Y
Y

Y
Y
Y

Y
Y
Y

16
9

Y
Y

Y
Y

Y
Y

15
12
20
15

Y
Y
Y
N

Y
Y
Y
N

Y
Y
N
N

11

17
3
12

N
N
Y

Y
N
Y

Y
N
Y

43
30
29
25

N
N
Y
Y

N
Y
Y
N

N
Y
N
Y

11

9
7
9

N
Y
Y

Y
Y
N

Y
Y
N

206

326
597
164
3599

Y
Y
Y
Y

N
N
N
N

N
N
N
N

92

nancy was monochorionic, a conservative approach following

single-twin death resulted in a 20% (12/60) intrauterine or
neonatal loss by rate by 4 weeks after delivery. Where the
pregnancy was dichorionic, this figure was 13% (5/38). There
was insufficient data concerning immediate delivery following
single-twin death.

Discussion and conclusion

In the majority of studies, data were not available concerning

the type of management strategy employed. Where the preg-

Single fetal death in a twin pregnancy is known to be a serious

complication of pregnancy. It is a relatively rare complication
of multiple pregnancies (5% of all twin pregnancies)15 but
may carry with it an increased risk of perinatal morbidity
and mortality. The main findings in this systematic review
are that following the death of one twin after the first trimester, the odds of intrauterine death of the co-twin and
neurological abnormality among survivors was six and four
times higher in monochorionic compared with dichorionic
pregnancies.
The main strength of this review is that it employed an
exhaustive research strategy. In this way, we were able to
assemble evidence for a condition that is rare and is imprecisely assessed in individual studies. In addition, the quality
of these studies was assessed together with stratification of
results according to chorionicity. However, the number of
studies where chorionicity has been indicated is relatively
small. It was also not possible to identify the relationship of
chorionicity to zygosity in the multiple pregnancy cohorts
described.
This systematic review includes more monochorionic than
dichorionic twins in the analysis of comparative data within
studies. This is a potential source of ascertainment bias given
that in a general population, two-thirds of twin pregnancies
are dichorionic. Furthermore, many of the studies were small
case series. Publication bias is an issue where individuals with
a case series of successful outcomes would be more likely to
report than other individuals with a similar case series of poor
outcomes.
These data do though provide clinicians and patients with
contemporary and reliable estimates of outcomes regarding
prognosis following single fetal death in a twin pregnancy.
However, due to poverty of reporting in individual studies,
these data cannot reliably guide clinicians regarding management, particularly issues concerning the timing of delivery
remain unexplored.
There are two theories that have been advanced to explain
multicystic encephalomalacia and co-twin death in monochorionic pregnancies. The first is that there is passage of
thrombotic material from the dead to healthy twin following
derangement in coagulation due to the death of one twin.35
The second theory is the haemodynamic imbalance theory.
This states that the placental anastomoses (frequently present
in monochorionic placentas) allow transfer of blood from the

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology

995

N, no; Y, yes.

this was not statistically significant (six studies; OR 1.91 [95%

CI 0.705.21] heterogeneity P = 0.20) (Figure 4).

Management strategy

Ong et al.

Well-defined sample at uniform stage

Gestational age of single-twin death

10

18

Prognostic factors considered

Chorionicity

23

15

Congenital anomalies

13

Follow up

28

Objective outcome
Death

28
10

18

Neurological

20

40

60

80

100%

No/unclear/not reported

Yes
Figure 2. Quality assessment of studies in systematic review.

two deaths and one case of neurological injury in known

dichorionic twins.
It is clear from this review that data has thus far been
poorly reported and that this area needs further robust

surviving twin to the dead co-twin giving rise to periods of

hypoperfusion, hypotension and acute fetal anaemia, resulting in neurological damage.36 In this systematic review, where
there was comparative data within studies, there were only
Co-twin in utero death

Neurological abnormality in survivor

Preterm delivery

Monochorionic

Monochorionic
Abdal-khalig and Sobande
10
Axt et al.
12
Bajoria et al.
30
Eglowstein and DAlton
21
Fusi and Gordon
26
Gaucherand et al.
32
Ishimatsu et al.
29
Jou et al.
15
Kilby et al.
9
Malinowski et al.
16
Petersen and Nyholm
19
Santema et al.
31
Sonneveld and Correy
2
Woo et al.

33

10

Axt et al.
12
Bajoria et al.
30
Eglowstein and DAlton
21
Fusi and Gordon
26
Gaucherand et al.
32
Ishimatsu et al.
29
Jou et al.
24
Lin et al.
16
Petersen and Nyholm
18
Saito et al.
20
van Heteren
25
Wang et al.
2
Woo et al.

n = 19
n=4
n = 50
n=8
n=8
n=6
n = 12
n = 12
n=7
n=4
n=5
n = 13
n=7
n=5

Monochorionic

n=4
n = 21
n=8
n=6
n=5
n=9
n=8
n=7
n=4
n = 14
n=9
n=9
n=4

10

Axt et al.
21
Fusi and Gordon
26
Gaucherand et al.
32
Ishimatsu et al.
29
Jou et al.
16
Petersen and Nyholm
18
Saito et al.
31
Sonneveld and Correy
20
van Heteren
25
Wang et al.
2
Woo et al.

Dichorionic
10

Axt et al.
12
Bajoria et al.
30
Eglowstein and DAlton
21
Fusi and Gordon
26
Gaucherand et al.
32
Ishimatsu et al.
24
Lin et al.
16
Petersen and Nyholm
18
Saito et al.
2
Woo et al.

Dichorionic
Abdal-khalig and Sobande
10
Axt et al.
12
Bajoria et al.
30
Eglowstein and DAlton
21
Fusi and Gordon
26
Gaucherand et al.
32
Ishimatsu et al.
15
Kilby et al.
9
Malinowski et al.
16
Petersen and Nyholm
1
Pharoah and Adi
28
Rydhstrom
19
Santema et al.
31
Sonneveld and Correy
2
Woo et al.

33

n = 16
n=3
n = 42
n = 11
n=8
n=2
n=3
n = 13
n=7
n=7
n = 181
n = 47
n = 16
n=9
n=1

n=3
n=7
n=5
n=9
n=7
n=5
n = 17
n=4
n = 11
n=7
n=2

Dichorionic
10

n=3
n = 33
n = 11
n=6
n=2
n=3
n=3
n=6
n = 10
n=1

Axt et al.
21
Fusi and Gordon
32
Ishimatsu et al.
16
Petersen and Nyholm
18
Saito et al.
31
Sonneveld and Correy

n=2
n=6
n=2
n=6
n=6
n=1

Undefined
Zorlu et al.

0.0

0.2

0.4

0.6

0.8

1.0

22

n=9

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

Figure 3. Forrest plots of outcomes for the surviving co-twin following single-twin death according to chorionicity.

996

RCOG 2006 BJOG An International Journal of Obstetrics and Gynaecology

Prognosis following single-twin death

Study

Monochorionic
n/ N

Dichorionic
n/ N

OR (fixed)
95% CI

OR (fixed)
95% CI

Co-twin death
Abdal-khalig and Sobande
10
Axt et al.
30
Eglowstein and DAlton
26
Gaucherand et al.
32
Ishimatsu et al.
15
Kilby et al.
16
Petersen and Nyholm
31
Sonneveld and Correy
9
Malinowski et al.
19
Santema et al.
2
Woo et al.
12
Bajoria et al.
21
Fusi and Gordon

33

Total (95% CI)

0/19
0/4
0/8
0/6
0/12
0/7
0/5
0/7
1/4
2/13
1/5
13/50
1/8

0/16
0/3
0/11
0/2
0/3
0/13
0/7
0/9
0/7
0/16
0/1
1/42
1/8

Not estimable
Not estimable
Not estimable
Not estimable
Not estimable
Not estimable
Not estimable
Not estimable
6.43 (0.21201.07)
7.17 (0.31163.82)
1.00 (0.0240.28)
14.41 (1.80115.53)
1.00 (0.0519.36)

148

138

6.04 (1.8419.87)

0/4
0/4
2/21
1/8
1/4
4/9
2/14
3/6
1/5
1/7

0/6
0/1
0/33
0/11
0/3
0/3
0/10
1/6
0/2
0/3

Not estimable
Not estimable
8.59 (0.39188.26)
4.60 (0.16128.54)
3.00 (0.09102.05)
5.73 (0.23142.55)
4.20 (0.1897.55)
5.00 (0.3472.77)
1.67 (0.0558.28)
1.62 (0.0551.11)

82

78

4.07 (1.3212.51)

5/5
6/9
13/17
2/3
2/4
4/7

3/6
1/2
2/6
2/2
1/1
4/6

45

23

Test for heterogeneity: P = 0.56, I = 0%

Test for overall effect: P = 0.003

Neurological abnormality
16

Petersen and Nyholm

2
Woo et al.
12
Bajoria et al.
30
Eglowstein and DAlton
10
Axt et al.
32
Ishimatsu et al.
18
Saito et al.
21
Fusi and Gordon
26
Gaucherand et al.
24
Lin et al.

Total (95% CI)

2

Test for heterogeneity: P = 1.00, I = 0%

Test for overall effect: P = 0.01

Preterm delivery
16

Petersen and Nyholm

32

Ishimatsu et al.
Saito et al.
Axt et al.

18

10
31

Sonneveld and Correy

21

Fusi and Gordon

Total (95% CI)

11.00
2.00
6.50
0.33
0.33
0.67

(0.43284.30)
(0.0944.35)
(0.8549.69)
(0.0112.82)
(0.0112.82)
(0.076.41)

1.91 (0.705.21)

Test for heterogeneity: P = 0.40, I = 1.9%

Test for overall effect: P = 0.20

0. 0 0 1 0. 0 1

0. 1

m o n oc h o r i o n i c b e t t e r

10

100

1000

d i c h o r i o n i c b et t e r

Figure 4. Meta-analysis of studies providing information of co-twin death, neurological abnormality and preterm delivery following single-twin
death after 14 weeks of gestation. A comparison of odds between monochorionic and dichorionic pregnancies.

1 Pharoah PO, Adi Y. Consequences of in-utero death in a twin pregnancy. Lancet 2000;355:1597602.
2 Woo HH, Sin SY, Tang LC. Single foetal death in twin pregnancies:
review of the maternal and neonatal outcomes and management.
Hong Kong Med J 2000;6:293300.

3 Cleary-Goldman J, DAlton M. Management of single fetal demise in

a multiple gestation. Obstet Gynecol Surv 2004;59:28598.
4 Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D,
et al. Meta-analysis of observational studies in epidemiology: a proposal
for reporting. Meta-analysis Of Observational Studies in Epidemiology
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5 Khan K, Riet GT, Glanville J, Sowden A, Kleijnen J. Undertaking Systematic Reviews of Research on Effectiveness. CRDs Guidance for
Carrying Out or Commissioning Reviews, 2nd edn. York, UK: NHS
Centre for Reviews and Dissemination, University of York, 2000.
6 Rennie D. Improving reports of studies of diagnostic tests: the STARD
initiative. JAMA 2003;289:8990.
7 Thompson SG. Why sources of heterogeneity in meta-analysis should
be investigated. BMJ 1994;309:13515.
8 Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining
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In: Egger M, Davey Smith G, Altman DG, editors. Systematic Reviews
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9 Malinowski W, Szymczykiewicz P, Pajszczyk-Kieszkiewicz T. Intrauterine death of one twin during the II trimester of a multiple pregnancy.
Ginekol Pol 2000;71:125561.

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997

research. There is a need for population-based data relating

to this obstetric complication with pregnancies being classified prospectively by chorionicity. In the UK, there are
a growing number of regional congenital anomaly databases
that report the incidence and prevalence of congenital
anomalies and relate this to denominator data for the background number of maternities. If multiple pregnancies were
reported and chorionicity was also recorded, robust population data would be available by which to assess further
these complications. j

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