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
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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).
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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
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Table 2. Prospective risk of IUFD per ongoing pregnancy in all twins by gestational age.
Monochorionic Dichorionic
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.
Monochorionic Dichorionic
Ongoing
pregnancies
Ongoing
pregnanciesProspective risk Prospective risk
Week of gestation n Percentage IUFD (n) of IUFD (%) n Percentage IUFD (n) of IUFD (%)
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
IUFD, in utero fetal death.
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).
Monochorionic Dichorionic
Ongoing
pregnancies
Ongoing
pregnanciesProspective risk Prospective risk
Week of gestation n Percentage IUFD (n) of IUFD (%) n Percentage IUFD (n) of IUFD (%)
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
IUFD, in utero fetal death.
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.
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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
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R. Mahony et al. Fetal death in twins
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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