Fetal Death in Twin

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M A I N R E S E A R C H A R T I C L E

Fetal death in twins

RHONA MAHONY1, CELIA MULCAHY1, FIONNUALA MCAULIFFE2, COLM O HERLIHY2, STEPHEN

CARROLL1 & MICHAEL E. FOLEY2

1Department of Obstetrics and Gynaecology, National Maternity Hospital and 2Department of Obstetrics and Gynaecology,University College Dublin, Dublin, Ireland

Key words

Twin pregnancy, fetal death, chorionicity,

intrauterine growth restriction, twin-twin

transfusion syndrome

Correspondence

Rhona Mahony MD, Consultant Obstetrician,

National Maternity Hospital,

Holles St, Dublin 2, Ireland.

E-mail: [email protected]

Conflict of interest

The authors have stated explicitly that there

are no conflicts of interest in connection with

this article.

Received: 24 January 2011

Accepted: 7 July 2011

DOI: 10.1111/j.1600-0412.2011.01239.x

Abstract

Objective. To examine the pattern and prospective risk of intrauterine fetal death

(IUFD) in twin pregnancy by chorionicity. Design. Retrospective cohort analysis.

Setting. Large national tertiary referral center. Population. All consecutive twin de-

liveries (1997–2006) ≥24 weeks. Methods . Retrospective review of all consecutive

twin deliveries over 10 years to identify patterns of IUFD in twins and calculate

gestation-specific prospective risks of IUFD. Fetal death was defined as intrauterine

demise of a fetus ≥24weeks, intertwin birthweight discordance as ≥20% differenceand growth restriction as birthweight <5th centile. Chorionicity was confirmed by

postnatal placental examination. Main outcome measures. Fetal death. Results. 1094

twin pairs including 276 monochorionic-diamniotic (MCDA) (25.3%) and 818

dichorionic-diamniotic (DCDA) twin pregnancies (74.7%) were studied. Twenty-

nine fetal deaths occurred affecting 22 twin pregnancies. The incidence of IUFD

(death of one or both fetuses) in MCDA twin pregnancies was three times that

in DCDA pregnancies [11/276 (3.9)% vs. 11/818 (1.3%) p <0.001]. The majority

of deaths in MCDA twins were associated with twin–twin transfusion syndrome

(TTTS) prior to 30 weeks. In normally grown twins the prospective risk of IUFD

was similarly low in MCDA and DCDA pregnancies after 34 weeks but in preg-

nancies complicated by abnormal growth, the prospective risk of IUFD was 3.4 in

MCDA and 2.0 in DCDA pregnancies. Conclusion. Twin pregnancies complicated

by growth restriction or growth discordance were associated with a high risk of IUFD, particularly in affected MCDA twins. Conversely, in normally grown twins

the risk was similarly low in MCDA and DCDA pregnancies after 34 weeks.

Abbreviations: DCDA, dichoriotic-diamniotic; IUFD, intrauterine fetal death;

MCDA, monochorionic-diamniotic; TTTS, twin twin transfusion syndrome.

Introduction

Perinatalmortality is increasedin twincomparedwith single-

ton pregnancies, and is greater in monochorionic diamniotic

(MCDA) compared with dichorionic diamniotic (DCDA)twins (1,2). Much of the excess fetal loss in twin pregnan-

cies can be attributed to preterm birth, intrauterine growth

restriction, and twin-to-twin transfusion in MCDA preg-

nancies (3). Intrauterine fetal death (IUFD) is particularly

devastating in monochorionic pregnancies because of the el-

evated risk of co-twin demise and the high risk of adverse

neurological outcome if the co-twin survives (4).

It has been shown that perinatal mortality in twin preg-

nancy reaches a nadir at around 38 weeks’ gestation and

rises thereafter (5), indicating that it may be unwise to pro-

long twin pregnancy much beyond 38 weeks. Indeed, some

authors suggest delivery of MCDA twins before 38 weeks

and the optimal timing of MCDA twins remains contro-

versial. Concern has been expressed that IUFD in MCDA

twins is increased and unpredictable (6). The inability to

identify the ‘at risk’ fetus has prompted a call for the evalua-

tionof elective preterm delivery in apparentlyuncomplicated

MCDA twins at around 36 weeks in an effort to reduce the

risk of unexpected stillbirth (7,8). It has been shown that

even when MCDA twin pregnancies affected by growth dis-

orders and twin-twin transfusion syndrome are excluded,

the excess risk of IUFD is maintained in apparently nor-

mal MCDA twin pregnancies, although a relatively small

1274C 2011 The Authors

Acta Obstetricia et Gynecologica Scandinavica C 2011 Nordic Federation of Societies of Obstetrics and Gynecology 90 (2011) 1274–1280

A C TA Obstetricia et Gynecologica



R. Mahony et al. Fetal death in twins

proportion of the MCDA cohort in this study proceeded

beyond 35 weeks (3).

Optimal managementinvolves a balance of risk, as even late

pretermdelivery is not withoutmorbidity and even mortality

(9). Like perinatal mortality, perinatal morbidity has been

shown to be lowest for twins born at 37–38 weeks (9). Our

aim was to perform a retrospective cohort analysis of alltwin deliveries at a single tertiary care center over 10 years

to determine the pattern of fetal death in twin pregnancy

according to chorionicity. We placed particular emphasis on

fetal deaths at or after 34 weeks’ gestation (elective routine

delivery is unlikely to be considered before this gestation).

In addition, in keeping with previous published data (3), we

have presented the prospective risk of fetal in death in both

MCDA and DCDA twins to facilitate comparison, as during

the course of this study we did not electively deliver twin

pregnancies prior to 38 weeks.

Material and methodsAll consecutive twin gestations delivered at the National Ma-

ternity Hospital Dublin from 1st January 1997 to 31st Decem-

ber 2006 were identified from the hospital perinatal database.

Inclusion criteria were twins with two viable fetuses at 23+6

and delivery at 24+0weeks or later. We excluded pregnancies

with fetal malformation, unknown chorionicity, monoam-

niocity and twin sets within triplets and higher order multi-

ples. Chorionicity was determined by placental histopatho-

logic examination rather than by ultrasound alone (10). Fetal

death wasdefined as intrauterine demiseof a fetus≥24weeks’

gestationand thestillbirthrate wascalculated as theincidence

of stillbirth per pregnancy. Growth restriction was defined asbirthweight<5th percentile for gestational age on a standard-

ized growth chart (11). Birthweight discordance was calcu-

lated by subtracting the weight of the smaller twin from that

of the larger twin and dividing the difference by the weight

of the larger twin and expressed it as a percentage. Signifi-

cant intertwin discordance was defined as 20% or greater (3).

Twin–twin transfusion syndrome (TTTS) was diagnosed ac-

cording to the internationally accepted sonographic criteria

adopted by the Eurofetus project (www.eurofetus.org): max-

imum vertical pocket of amniotic fluid (MVP) <2cm in the

donor’s gestational sac and an MVP ≥8cm in the recipient’s

sac (≥10cm in the recipient’s sac after 20 weeks’ gestation),

with distended bladder in the recipient and collapsed bladder

in the donor in most of the examinations (12).

Gestational age-specific stillbirth rates per twin pregnancy

were calculated as the incidence of fetal death per pregnancy

(whether single or double) during or after a given two-week

gestational period divided by the total number of ongoing

pregnancies at thestart of theperiod(3). In concordancewith

a previous study, twins were classified as apparently ‘normal

growth’ in the absence of IUGR, significant inter-twin dis-

cordance and TTTS (3). Conversely, ‘abnormal growth’twins

were defined as twin pregnancies complicated by IUGR or

significant growth discordance excluding TTTS.

Statistical analysis was performed using the spss statistical

package (SPSS Inc., Chicago, IL, USA). Differences between

categorical variables were analyzed using the chi-squared test

and differences between continuous variables were summa-rized as means and standard deviations. Groups were com-

pared using Student’s t -test. All hypothesis tests were two-

sided and significance was set at <0.05. As this study con-

formed to the standards established by the National Health

and Research Council for ethical quality review, specific ethi-

calapproval was notrequired because all of the data obtained

retrospectively were in the public domain and published an-

nually in the hospital clinical reports.

Results

During the 10-year study period, 1 178 twin pairs were deliv-

ered at NMH. Ten twin pairs were excluded because of inade-quate data. Data on placental chorionicity were not available

in 74 twin pairs (6.3%) leaving 1 094 twin pregnancies as

the subject of this study, including 276 monochorionic twin

pairs (25.3%) and 818 dichorionic twin pairs (74.7%).

Monochorionic twins were delivered significantly earlier

than dichorionic twins, although there was no difference in

the incidence of growth discordance or IUGR between the

two groups (Table 1); 164/276 (59.4%) of MCDA twins de-

livered at or after 36 weeks’ gestation compared with 626/818

(76.5%) of DCDA twins ( p <0.001). Of the 112 MCDA and

192 DCDA twin pairs who were delivered before 36 weeks’

gestation, 63.6% of theMCDA twins and 71.6% of the DCDA

twins were delivered following spontaneous preterm labor.

Conversely, 36.4% of MCDA and 28.4% of DCDA twins were

delivered prelabor in the fetal or maternal interest. Overall,

Table 1. Characteristics of 1 094 twin pregnancies in NMH in 1997–

2006 analyzed by chorionicity.

Monochorionic Dichorionic

n = 276 n = 818 p

Mean gestation/(weeks) at

delivery

35 ± 3.7 36 ± 2.88 <0.001

Mean birth weight/g 2319 ± 36 2584 ± 615 <0.001

Birthweight < 5th

percentile/pregnancy46 (16.6%) 159 (19.4%) 0.35

Growth discordance

>20%/pregnancy

54 (19.6%) 144 (17.6%) 0.52

Stillbirth/pregnancy 11 (3.9%) 11 (1. 34%) 0.01

Stillbirth/‘normal growth

pregnancy’ (IUGR,

growth discordance,

TTTS excluded)

1/194 (0.5%) 6/575 (0.87%) 1

Data are expressed as n, n (%) or mean (±SD).

C 2011 The Authors

Acta Obstetricia et Gynecologica Scandinavica C 2011 Nordic Federation of Societies of Obstetrics and Gynecology 90 (2011) 1274–1280 1275



Fetal death in twins R. Mahony et al.

the incidence of intrauterine fetal death (IUFD) per preg-

nancy (whether single or double) in MCDA twins was three

times that in DC twins [11/276 (3.9)% vs. 11/818 (1.3%)

p <0.001) (Table1). Whenpregnanciescomplicated by TTTS,

growth discordance and/or IUGR were excluded (‘normal

growth pregnancies’), the overall incidence of IUFD wassim-

ilar in MCDA and DCDA pregnancies [(1/194 (0.5%) vs.6/575 (0.87%); p =1.0] (Table 1).

The number of fetal deaths by gestational week and the

prospective risk of IUFD with increasing gestation is shown

for all twins studied in Table 2. The prospective risk of IUFD

in alltwins was greater in MCDA than DCDA twins at allges-

tations after 24 weeks with the risk being greatest between 24

and 27 weeks in MCDA twins (Table 2). After 34 weeks’ ges-

tation, the incidence of IUFD was 2/205 (0.97%) in MCDA

twins vs. 6/708 in DCDA twins (0.85%) ( p =1.0). In ap-

parently ‘normal growth’ twins, there was only one IUFD

at 26 weeks’ gestation in MCDA twins compared with six

antepartum deaths in 575 DCDA pregnancies. At or after

34 weeks, there were two deaths of 489 ongoing pregnancies

in normally grown DCDA twins and no deaths in normally

grown MCDA twins (Table 3). In twin pregnancies affected

by growth discordance or IUGR (but TTTS excluded), i.e.

‘abnormally grown’ twin pregnancies, the prospective risk

of IUFD in MCDA twins was greater at all gestations. At

34 weeks’ gestation the prospective risk of IUFD was 3.4 in

MCDA pregnancies and 1.8 in DCDA pregnancies, rising

to 4.3 and 2.0, respectively, at 36 weeks’ gestation ( p =0.33)

(Table 4).

Of 11 instances of IUFD in MCDA twin pregnancies, five

(45.4%) were double deaths and of 11 IUFDs in DCDA preg-

nancies, two (18.1%) were double deaths. The individualcauses of IUFD are detailed in Table 5. The majorityof deaths

in MCDA twins, 8/11 (72.7%), were related to TTTS, with

two cases of IUFD related to placental abruption at 37 weeks’

gestation.In oneof these cases,the fetuses were discordant for

growth and in the other, both fetuses were growth-restricted.

Seven of 13 deaths in DCDA twins were related to IUGR or

growthdiscordance(Table5).Overall,sixofeightcases(75%)

of IUFD in all twin pregnancies at or after 34 weeks’ gestation

(2/2 MCDA and4/6 DCDA pregnancies)were associated with

either growth discordance or IUGR. After 34 weeks the inter-

val between last scan and diagnosis of IUFD was one week or

less in all cases, except one case of DCDA twins where there

had been a four-week interval between scan and diagnosis

of IUFD. In the MCDA group, a late double fetal death oc-

curred at 37 weeks. In this case, amniotomy was performed

to induce labor because of IUGR. Amniotomy was followed

by placental abruption and the demise of both fetuses. In the

DCDA group of twins, three pregnancieswere affected by late

IUFD (including one double death) at ≥38 weeks’ gestation.

In total, there were 16 stillbirths and 14 neonatal deaths in

the MCDA twins and 13 stillbirths and 22 neonatal deaths

in the DCDA twins. This gives a perinatal mortality rate of

54/1 000 in the MCDA twins and 21/1 000 in the DCDA

twins ( p <0.001). In MCDA twins 13/14 neonatal deaths and

in DCDA twins 16/22 deaths occurred before 26 weeks’ ges-

tation and were related to prematurity.

Discussion

ThiswasalargeretrospectivestudyofIUFDinover1000twin

pregnancies in which the majority delivered after 36 weeks’

gestation (59% in MCDA twins and 76% in DCDA twins).

The overall risk of IUFD was threefold greater in MCDA than

DCDA twins and the prospective risk of IUFD was greater in

MCDA twin pregnancies at all gestations after 24 weeks, con-

sistent with previous studies (2). In addition, the proportion

of twin pregnancies affected by double fetal death was greater

in MCDA twin pregnancies, consistent with the elevated risk

of co-twin death in MCDA pregnancies because of placenta

vascular anastomoses. Almost three-quarters of all deaths

in MCDA twins occurred before 30 weeks’ gestation and

were related to TTTS. In apparently normally grown twins,

the risk of IUFD was similarly low in MCDA and DCDA

twin pregnancies. In contrast, in twin pregnancies compli-

cated by IUGR, growth discordance or both, the prospective

risk of IUFD was higher than in apparently normal grown

twins, with the highest prospective risk of IUFD occurring

in abnormally grown MCDA twins. After 34 weeks’ gesta-

tion, three-quarters of deaths were associated with IUGR or

growth discordance with a prospective risk of 3.4% in ab-

normally grown MCDA twins vs. 2.0% in abnormally grown

DCDA twins. These data are consistent with recently pub-

lished information (13).When TTTS is excluded, the majority of deaths in MCDA

twins and almost half the deaths in DCDA twins were as-

sociated with IUGR and/or growth discordance. We were

only able to identify one IUFD in MCDA twins with ap-

parently normal growth and this was associated with vasa

previa. At or after 34 weeks’ gestation, the two of two cases

of IUFD in MCDA twins were associated with abnormal

growth, while four of six cases of IUFD in DCDA twins at

or after 34 weeks’ gestation were associated with growth dis-

cordance or IUGR. Birthweight discordance affects up to

30% of twin pregnancies and has long been associated with

adverse perinatal outcome (14,15,16). Different genetic po-

tential, crowding in utero, and placental insufficiency have

been postulated to cause discordant growth in dichorionic

twins, whereas unequal sharing of placental mass and hemo-

dynamic imbalance caused by placental vascular anastomoses

is commonly cited as the etiology of growth discordance in

monochorionic twins (17,18). The risk of adverse perinatal

outcome has been shown to increase when growth discor-

dance in twins is associated with IUGR (19–21). Our results

are consistent with this finding, showing that even when






Table 2. Prospective risk of IUFD per ongoing pregnancy in all twins by gestational age.


Ongoing

pregnancies

Ongoing

pregnanciesProspective risk Prospective risk

Week of gestation n Percentage IUFD (n) of IUFD (%) n Percentage IUFD (n) of IUFD (%)

24–25 276 100 2 3.9 818 100 1 1.34

26–27 268 97.1 4 3.4 810 99.0 0 1.23

28–29 255 92.4 2 1.9 800 97.8 1 1.25

30–31 245 88.8 0 1.2 786 96.0 1 1.0

32–33 231 83.6 1 1.3 754 92.2 2 1.1

34–35 205 74.2 0 1.0 708 86.5 1 0.8

36–37 164 59.4 2 1.2 626 76.5 2 0.79

≥38 84 30.4 0 - 241 29.4 3 1.2

IUFD, in utero fetal death.

Prospective risk of IUFD was calculated as the incidence of stillbirths per pregnancy (whether single or double) during or after a given two-week

gestational period divided by the total number of ongoing pregnancies at the start of the time period.

Table 3. Prospective risk of IUFD per ongoing pregnancy in ‘apparently normally grown’ twins by gestational age.


Ongoing

pregnancies

Ongoing



24–25 194 100 0 1.03 575 100 1 1.04

26–27 190 97.9 1 1.05 569 98.9 0 0.87

28–29 180 92.7 0 0.55 560 97.3 1 0.89

30–31 175 90.2 0 - 546 94.9 1 0.73

32–33 164 84.5 0 - 521 90.4 1 0.57

34–35 146 75.3 0 - 489 85.0 1 0.40

36–37 118 60.8 0 - 426 74.1 0 0.23

≥38 67 34.5 0 - 240 41.7 1 0.41


Prospective risk of IUFD was calculated as the number of stillbirths per pregnancy during or after a given two-week gestational period divided by the

total number of ongoing pregnancies at the start of the time period.

Table 4. Prospective risk of IUFD per ongoing pregnancy in ‘abnormally grown’ twins by gestational age (TTTS excluded).


Ongoing

pregnancies

Ongoing



24–25 80 100 0 2.5 243 100 0 2.0

26–27 75 95.1 0 2.6 241 99.2 0 2.2

28–29 73 91.5 0 2.7 240 98.7 0 2.0

30–31 70 85.4 0 2.8 240 98.7 0 2.0

32–33 66 81.7 0 3.0 233 95.8 1 2.1

34–35 59 71.9 0 3.4 219 90.1 0 1.8

36–37 46 56.0 2 4.3 200 82.3 2 2.0

≥38 17 20.7 0 2 0.8 2


Prospective risk of IUFD was calculated as the number of stillbirths per pregnancy during or after a given two-week gestational period divided by the

total number of ongoing pregnancies at the start of the time period.

C 2011 The Authors





Table 5. Intrauterine fetal death cases.

Gestation n Cause Birthweight Interval scan – IUFD

Monochorionic twin pregnancy

25, 1 (2) TTTS 880g, 720g 1 week

25 1 (2) TTTS 445g, 505g 1 week

26 1 TTTS 585g, 2 500g (at 38/40 weeks). 2 weeks

26 1 Unexplained 830g, 740g <1 week26 1 (2) TTTS 770g, 900g 2 weeks

27 1 TTTS 800g, 1 080g 1 week

28 1 (2) TTTS 645g, 880g∗ 2 weeks

29 1 TTTS 1 125g, 1230g 1 week

33 1 TTTS 3 430g,1730g∗ 4 weeks

37 1 Abruption 3 520g, 2740g∗ <1 week

37 1 (2) Abruption 2 205g, 1950g∗ <1 week

Dichorionic twin pregnancy

25 1 (2) Fetomaternal hemorrhage 920g, 790g <1 week

28 1 Pre-eclampsia 1 020g, 1 140g <1 week

30 1 Cholestasis 1 885g, 1 780g Ext Ref (external referral)

33 1 Vasa previa 1 700g, 2 130g 1 week

33 1 Growth discordance 1 580g, 2 260g <1 week∗

35 1 Unexplained 2 485g, 2 175g 1 week

36 1 IUGR 2 140g, 1 675g <1 week∗

37 1 IUGR 2 980g, 1 430g 4 weeks∗

38 1 (2) IUGR 3 530g, 2 100g 1 week∗

38 1 IUGR 2 495g, 2 420g 1 week∗

40 1 Unexplained 3 260g, 2 700g 1 week

∗Growth discordance >20% or IUGR.

n represents the number of twin pregnancies affected by stillbirth. (2) signifies death of both fetuses.

TTTS is excluded, three-quarters of IUFDs in all twins are

associated with growth restriction or growth discordance at

or after 34 weeks’ gestation. Ideally, twins with growth dis-cordance or IUGR should be identified by antenatal fetal

surveillance but it is widely acknowledged thatthe estimation

of fetal weight by ultrasound can vary within a range of up to

20% of the actual birthweight and is less accurate in multiple

pregnancies (22,23). In contrast, in normally grown twins,

there was only one death in MCDA twins at 26/40 weeks’

gestation, a finding consistent with previous studies (23,24).

It is noteworthy that more than half of all deaths (6/11) in

DCDA twins occurred in apparently normally grown DCDA

twins, with two of these deaths occurring after 34 weeks.

The greatest prospective risk of IUFD in MCDA twins oc-

curs between 24 and 27 weeks’ gestation, coinciding with

the greatest incidence of TTTS, which accounted for almost

three-quarters of all deaths in MCDA twins. Approximately

10–15% of monochorionic twin pregnancies are complicated

by TTTS and before 26 weeks of gestation this is associated

with a high risk of fetal loss, perinatal death and subsequent

handicap in survivors (25). Over the 10-year course of this

study, there have been many advances in the management

of TTTS which are likely to improve outcomes in MCDA

twins. At present, fetoscopic laser ablation of placental vas-

cular anastomoses appears to be the best first line treatment,

maximizing perinatal survival and minimizing long-term

neurodevelopment morbidity (26,27,28). One of the limi-tations of this study is the lack of prospectively recorded data

regarding the treatment of identified cases of TTTS. This 10-

year study began with the year 1997, a time when fetoscopic

laser coagulation was a new procedure restricted to a mi-

nority of centers. Although several affected pregnancies were

treated with amniodrainage, the data were not reliable and

were therefore omitted from this study.

Another limitation of this study is that it spanned 10 years

(1997–2006) during which there were significant advances in

the understanding of the particular challenges faced in the

management of twin pregnancy. Nonetheless, the data relate

to a very large cohort of twin pregnancies in whom the ma-

jority were delivered after 36 weeks. The findings have led

to a change in practice in keeping with current international

norms(22).ItisnowourpolicytoroutinelydeliverallMCDA

twins at 37 weeks and all DCDA twins at 38 weeks or ear-

lier if indicated. In addition, during this study, surveillance

of twin pregnancies has changed. Prior to 2002, chorionicity

was not routinely assigned and all twins were scanned every

four weeks. Ongoing audits prompted our unit to increase

fetal surveillance so that, at present, chorionicity is assigned






ultrasonically at 12 weeks’ gestation in all twin pregnancies.

MCDA twins are routinely scanned at least every two weeks

and DCDA twins every four weeks until 28 weeks’ gestation

and every two weeks after that. Each ultrasonic assessment

includes estimated fetal weight, biophysical score and umbil-

ical artery Doppler studies. It is possible that some of the late

fetal deaths highlighted in growth-restricted fetuses couldhave been avoided with more intensive fetal monitoring.

A further limitation in this study was theinabilityto deter-

mine exactly the timing of intrauterine death and the effect of

maceration on fetal weight (23). However, in the majority of

fetal deaths studied, we can reasonably exclude a prolonged

interval between intrauterine death and delivery so that it is

unlikely that intrauterine death could entirely account for the

birthweight discordance observed.

In conclusion, the majority of deaths in MCDA twins were

associated withTTTS. In the absence of TTTS, twin pregnan-

cies complicated by growth restriction or growth discordance

were associated with a high prospective risk of IUFD, with

the highest risk occurring in MCDA twins. Conversely, in

normally grown twins, the risk of IUFD was similarly low in

MCDA and DCDA pregnancies after 34 weeks.

Funding

No specific funding.

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Fetal Death in Twin

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