International Journal of Gynecology and Obstetrics (2007) 96, 98–102

a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m

w w w. e l s e v i e r. c o m / l o c a t e / i j g o

CLINICAL ARTICLE

Twin chorionicity and the risk of adverse

perinatal outcome
R. Acosta-Rojas a,c,⁎, J. Becker a , B. Munoz-Abellana a , C. Ruiz b ,
E. Carreras a , E. Gratacos a,c
for the Catalunya and Balears Monochorionic Network 1
a
Unitat de Medicina Fetal, Servei d'Obstetrícia, Hospital Materno-Infantil Vall d'Hebron, Barcelona, Spain
b
Servei de Neonatologia, Hospital Materno-Infantil Vall d'Hebron, Barcelona, Spain
c
Fetal Medicine Research Group, Obstetrics Department-ICGON, Hospital Clínic-IDIBAPS, Barcelona, Spain

Received 30 August 2006; received in revised form 29 October 2006; accepted 1 November 2006

KEYWORDS Abstract
Incidence;
Monochorionic twins; Objective: To evaluate the impact of chorionicity on the perinatal outcomes of twin pregnancies
Selective intrauterine complicated by twin–twin transfusion syndrome (TTS) or selective intrauterine growth restriction
growth restriction; (sIUGR). Method: Pregnancies with 127 monochorionic (MC) and 109 dichorionic (DC) twins were
Twin pregnancy; followed up, and TTS and sIUGR incidence as well as morbidity and mortality were evaluated.
Twin–twin transfusion Results: The incidence of intrauterine fetal death was higher in MC than in DC pregnancies (6.5%
syndrome vs. 1%), and higher in MC pregnancies complicated by TTS (5 deaths in 10 pregnancies [50%]) or sIUGR
(2 in 9 [22%]). The incidence of sIUGR was similar in MC and DC pregnancies (7% vs. 5%), and the
incidence of TTS was 8% in MC pregnancies (95% confidence interval, 3.2–12.8). Neonatal neuro-
logical and respiratory morbidity was higher among MC twins, and the increase in neonatal com-
plications was linked to TTS and sIUGR. Uncomplicated MC and DC pregnancies had similar perinatal
outcomes. Conclusion: The incidence of neonatal complications was higher in MC twins born of
pregnancies complicated by TTS or sIUGR. Although the incidence of sIUGR was similar in MC and DC
pregnancies, there was a trend towards worse outcomes in MC pregnancies affected by sIUGR.
© 2006 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd.
All rights reserved.

⁎ Corresponding author. Fetal Medicine Research Group, Departament d'Obstetrícia, Hospital Clínic, Sabino de Arana 1, Ed. Helios, 08028
Barcelona, Spain. Tel.: +34 93 227 9333; fax: +34 93 227 9336.
E-mail address: eracosta@clinic.ub.es (R. Acosta-Rojas).
1
The Catalunya and Balears Network also includes Astor J. (Hospital General de Granollers, Spain); Albaiges G. (Hospital H. Joan XXIII,
Tarragona, Spain); Cavalle P. (Hospital St. Joan de Reus, Spain); Bach C. (Hospital Josep Trueta, Girona, Spain); Martínez M. (Hospital St. Joan
de Déu, Martorell); Ros N. (Hospital Sta. Tecla, Tarragona, Spain); Rubio R. (Hospital del Mar, Barcelona, Spain); Torrents M. (Institut Dexeus,
Barcelona, Spain); Rodríguez S. (Hospital de Terrassa, Spain); Perapoch J., Cabero L., and Hermosilla E. (Hospital Materno-Infantil Vall
d’Hebron, Barcelona); Padilla N. (Fetal Medicine Research Group, Obstetrics Department-ICGON, Hospital Clínic-IDIBAPS).

0020-7292/$ - see front matter © 2006 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd.
All rights reserved.
doi:10.1016/j.ijgo.2006.11.002
Twin chorionicity and the risk of adverse perinatal outcome 99

1. Introduction 2. Material and methods

Monochorionic (MC) twin pregnancies are less frequent than This prospective study was conducted within a large research
dichorionic (DC) twin pregnancies, and are associated with project on MC twin pregnancies based on 127 MC and 109 DC
higher morbidity and mortality [1] long attributed to the pregnancies. The study protocol was approved by the institutional
existence of feto-fetal placental anastomoses in the mono- ethics committees of the participating institutions and informed
chorionic placenta [2,3]. Until recently twin-to-twin transfu- consent was obtained from all participants. Two cohorts of twin
sion syndrome (TTS) and single fetal death, which carries a pregnancies were followed up from a GA of 12th week through the
greater risk for the co-twin in MC than in DC pregnancies, were neonatal period (28 days). Women pregnant with monochorionic
considered the 2 conditions responsible for the poorer outlook twins were identified on routine ultrasonographic examination
of MC twin pregnancies [4–6]. Recent reports, however, have between the 11th and 14th weeks and recruited consecutively
suggested that selective intrauterine growth restriction from the centers participating in the study. Women pregnant with
(sIUGR) is also a condition associated with an increased risk dichorionic twins were recruited consecutively during the same
of intrauterine fetal death (IUFD) for one or both twins, and an period at the coordinating institution only. Twin pregnancies were
increased risk of neurologic morbidity in the larger twin classified as MC or DC by ultrasonographic criteria [11], and the
regardless of whether the fetus with IUGR survives [7]. characteristic was verified after delivery by examination of the
Selective intrauterine growth restriction has been reported placenta. Gestational age was calculated from the last menstrual
to occur in 12% to 25% of all MC pregnancies [8,9], and this wide period and confirmed ultrasonographically. All cases were
variation is due to the lack of a uniform definition. In most followed up according to a similar protocol, consisting essentially
studies, sIUGR is defined as one twin having an estimated fetal in ultrasonographic examinations at 2-week intervals.
weight (EFW) below the 10th or 5th percentile for gestational The following variables were recorded: incidence of TTS,
age (GA) while the other twin grows normally. Furthermore, sIUGR, and IUFD for both or one fetus (in cases of fetal loss);
most recent studies evaluating the impact of sIUGR on delivery before the 32nd and the 37th weeks of gestation; and
pregnancy outcome have included the inter-twin weight birth weight below the 5th percentile for GA in one or both
discordance, which seems to better identify cases with the fetuses, adjusted for normal twin and newborn values in the
highest risk of complications [7,10]. The incidence of sIUGR, Spanish population [12].
defined as a twin with an EFW below a predetermined sIUGR was calculated according to the following formula:
percentile for GA in one twin combined with a predetermined
inter-twin weight discordance, has not been evaluated. ðweight of the larger twin − weight of the smaller twinÞ
This study evaluated the impact of chorionicity on sIUGR  100=weight of the larger twin:
incidence and perinatal outcomes in twin pregnancies with
TTS. Inter-twin growth discordance was defined as one twin TTS was defined according to the Eurofetus criteria [13]. Twin
having an EFW below the 10th percentile for GA, with the pregnancies with chromosomal or congenital malformations
inter-twin growth discordance greater than 25%. were excluded from final analysis.
All newborns were evaluated following the same protocols.
Neonatal morbidity was recorded in all cases by the group's
pediatrician (C.R.). It was defined as the presence of at least one
of the following: neurological morbidity; signs of intraventricular
Table 1 Perinatal outcomes of monochorionic and di-
hemorrhage; periventricular leukomalacia; cerebral infarction
chorionic twin pregnancies
on neonatal ultrasonographic brain scan performed during the
Pregnancies Monochorionic Dichorionic P first 28 days of life; cardiovascular morbidity as a sign of
value persistent ductus arteriosus; persistent low output syndrome and
Gestational age at N = 123 N = 106 hypertrophic myocardiopathy; pulmonary morbidity with a need
delivery (weeks) for mechanical ventilation; respiratory distress syndrome or signs
suggesting broncho-pulmonary dysplasia; and intestinal morbid-
Mean (SD) 35.3 (3.4) 36 (2.7) 0.003
ity such as necrotizing enterocolitis or intestinal perforation.
Fetal loss
Differences in pregnancy outcome and neonatal morbidity
One 7/123 (6%) 1/106 (1%) 0.052
were compared between the 2 cohorts, and a subanalysis was
Both 1/123 (1%) 0 0.537
performed to evaluate the same variables in complicated and
At least one 8/123 (6.5%) 1/106 (1%) 0.03
uncomplicated pregnancies. Comparison between groups was
Preterm delivery
performed using, as appropriate, the t-test, analysis of variance
Delivery<37 weeks 91/123 (74%) 71/106 (70%) 0.155
with the Bonferroni correction, and the 2-sided Fisher exact test
Delivery<32 weeks 17/123 (14%) 9/106 (9%) 0.145
at the 5% level of significance; 95% confidence intervals (CIs)
Birthweight (g)
were calculated for the incidence. All statistical analyses were
Larger fetus
performed using the software package SPSS, version 13.0 (SPSS
Mean (SD) 2238 (576) 2420 (499) 0.002
for Windows, SPSS Inc, Chicago, Illinois, USA).
Smaller fetus
Mean (SD) 1926 (594) 2112 (463) 0.001
Birthweight 12/115 (10%) 12/105 (11%) 0.431 3. Results
discordance > 25%
One fetus BW < p5 33/122 (27%) 30/101 (28%) 0.386 Four of the 127 MC and 3 of the 109 DC pregnancies identified
⁎P value calculated by Student's t-test and Fisher's exact test. were later diagnosed with chromosomal or congenital
malformations and excluded from further analysis.
100 R. Acosta-Rojas et al.

Table 2 Perinatal outcomes in subgroups of monochorionic and dichorionic twin pregnancies

Monochorionic Dichorionic
N = 123 N = 106
Uncomplicated TTS sIUGR Uncomplicated sIUGR
Pregnancies (n) 104 10 9 101 5
85% 8% 7% 95% 5%
Gestational age at delivery ⁎ ⁎ ⁎ ⁎
(weeks)
Mean (SD) 36.0 (2.6) 33.3 0.001 31.3 0.001 35.7 (2.7) 1.000 33.3 1.000
(3.8) (2.7) (3.7)
Fetal loss
One 1/104 (1%) 4/10 0.001 2/9 0.016 1/101 (1%) 0.744 0
(40%) (22%)
Both 0 1/10 0.088 0 0 0
(10%)
At least one 1/104 (1%) 5/10 0.001 2/9 0.016 1/101 (1%) 0.744 0
(50%) (22%)
Preterm delivery
Delivery < 37 weeks 78/104 (75%) 5/9 0.188 7/9 0.607 66/101 (69%) 0.087 5/5 0.249
(56%) (78%) (100%)
Delivery < 32 weeks 10/104 (10%) 4/9 0.013 2/9 0.244 9/101 (9%) 0.527 0
(44%) (22%)
Birthweight (g)
Larger fetus
Mean (SD) 2376 (484) 2056 1.000 2186 1.000 2450 (520) 1.000 2266 1.000
(722) (684) (232)
Smaller fetus
Mean (SD) 2120 (463) 1136 0.021 1497 0.030 2180 (494) 1.000 1586 0,08
(645) (537) (207)
One fetus BW < p5 25/103 (24%) 3/5 0.108 6/7 0.002 27/95 (28%) 0.308 3/5 0.108
(60%) (86%) (60%)
⁎P value as compared to uncomplicated MC, calculated by Chi squared and Anova and Bonferroni test. Twin-to-twin transfusion syndrome
(TTS). Selective intrauterine growth restriction (sIUGR).

Perinatal outcomes for the MC and DC pregnancies are
summarized in Table 1. Overall, there were no significant
differences between these 2 groups in the incidence of
preterm delivery before the 32th and the 37th weeks; birth
weight below the 5th percentile for GA in one or both
fetuses; and birth weight discordance greater than 25%. The
incidence of IUFD was significantly higher in MC pregnancies
but that of sIUGR was similar in the 2 groups (7% [95% CI,
1.94–12.1] vs. 5% [95% CI 0.8–9.25]), respectively. In MC
pregnancies the TTS incidence was 8% (95% CI, 3.2–12.8). All
cases were treated with fetoscopic laser coagulation.
Perinatal outcome is shown in Table 2. Overall, uncom-
plicated MC and DC pregnancies had similar outcomes. A
higher incidence of IUFD was observed in pregnancies
complicated by TTS (5 of 10 [50%]) or sIUGR (2 of 9 [22%]).
Preterm delivery before the 32th week was higher in MC
pregnancies with TTS or sIUGR. When sIUGR was present,
similar GA at delivery and birth weight of both fetuses were
observed for MC and DC pregnancies. Although the number
was too small for statistical comparisons, the results showed
a trend for an increased incidence of IUFD in MC pregnancies
(2 of 9 [22%]) vs. 0 of 5 [0%]).
A subanalysis was performed on MC pregnancies with an
EFW below the 5th percentile in one twin, but with a birth
weight discordance below 25% (n = 25). These pregnancies'
outcomes were similar to those of the uncomplicated MC
pregnancies: (the mean ± SD gestational age at delivery was
37 ± 2.5 weeks; there were 4% and 60%, respectively, of
preterm deliveries before the 32th and the 37th week; and
there were no fetal losses).
Between 3% and 7% of the twins were not delivered in the
expected institution and neonatal information could not be
retrieved. Three neonatal deaths were observed, 2 following
TTS and 1 following sIUGR. Therefore, neonatal complica-
tions are based on 220 MC and 205 dichorionic twins. The
incidence of neonatal complications is shown in Table 3. Need
for admission in the neonatal intensive care unit (NICU) was
greater for monochorionic than for dichorionic twins (19% vs.
12%; P = 0.032). There was a higher incidence of neurologic
(3% vs.0.5%; P = 0.042) and respiratory (14% vs. 8%; P = 0.027)
morbidity among monochorionic twins, and when neonatal
complications were analyzed by subgroups, TTS and sIUGR
accounted for the higher morbidity. Morbidity was similar in
uncomplicated MC and DC pregnancies (Table 4).
4. Discussion
This prospective cohort study provides information on the
natural history of MC twin pregnancies. The rate of IUFD was
globally increased in MC pregnancies compared with DC
Twin chorionicity and the risk of adverse perinatal outcome 101

Table 3 Neonatal morbidity in monochorionic and have often been reported as separate variables in epidemio-
dichorionic twin pregnancies logical studies on twins [14,15]. The combination of the 2
criteria seems to better identify the subgroup of fetuses with
Children (n) Monochorionic Dichorionic P a higher risk of death in utero [16]. Differences in feto-
value placental blood volume, in combination with inter-twin
220 205 placental anastomoses, have been reported to account for
NICU 41/220 (19%) 24/205 (12%) 0.032 an increased risk of acute feto-fetal transfusion accidents in
Morbidity MC pregnancies [17]. In the present study, this condition was
Neurological 7/220 (3%) 1/205 (0.5%) 0.042 associated with an increase in IUFD that could not be
Periventricular 0 0 attributed to TTS. In contrast, fetal weight below the 5th
Leukomalacia percentile as an isolated finding occurred with a much higher
Intraventricular 6/220 (3%) 1/205 (0.5%) 0.073 incidence, but this was associated with outcomes similar to
hemorrhage the outcomes of uncomplicated MC pregnancies. Although
Cerebral infarction 1/220 (0.4%) 0 0.518 the small size of the subgroups does not allow to establish
Respiratory 31/220 (14%) 16/205 (8%) 0.027 reliable estimations, the 22% mortality rate MC pregnancies
Mechanical 18/220 (8%) 9/205 (4%) 0.080 with sIUGR is similar to the 17% [19] previously reported in a
ventilation larger sample with the same diagnosis. These rates are lower
Bronchopulmonary 8/220 (4%) 0 0.005 than the 41% reported by Quintero and colleagues [7].
dysplasia However, in that series the authors included only severe
Gastrointestinal 9/220 (4%) 4/205 (2%) 0.159 forms of sIUGR, i.e., fetuses with absent or reversed end-
Necrotizing 5/220 (2%) 3/205 (1%) 0.402 diastolic flow in the umbilical artery.
enterocolitis The TTS incidence of 8% was in keeping with the 10.6%
Cardiovascular 14/220 (6%) 6/205 (3%) 0.073 reported in a recent population-based study [18], but lower
Persistent ductus 6/220 (3%) 0 0.019 than the 15% reported by Sebire and colleagues [19]. The risk
arteriosus of TTS is the main reason for a closer follow-up in MC
NICU = need of neonatal intensive care unit. pregnancies.
P value, calculated by Fisher's exact test. The 1% observed incidence of IUFD is very similar to that
reported in two recent prospective studies evaluating the risk
of fetal death in uncomplicated MC twin pregnancies. In
agreement with the data here reported, Simoes and associ-
pregnancies. Poor perinatal outcome accumulated in cases ates [20] reported an incidence of 2.6%; but as only 1.2%
presenting either TTS or sIUGR, while uncomplicated MC and occurred after 32 weeks of pregnancy, they concluded that
DC pregnancies had similar perinatal outcomes. elective preterm delivery in these pregnancies was not
Although the incidence of sIUGR, as defined in this study, justified. A higher IUFD incidence has been reported by
was not different for MC and DC pregnancies (7% and 5%, Barigye and coworkers [21], who observed an overall 4.6% risk
respectively), sIUGR was linked to a higher rate of perinatal per pregnancy, 4.3% after 32 weeks. However, signs of late-
and neonatal complications in MC pregnancies. Growth onset TTS were observed in at least 2 of their cases [21], which
retardation in one twin and inter-twin weight discordance would reduce the risk in truly uncomplicated pregnancies to

Table 4 Neonatal morbidity in subgroups of monochorionic and dichorionic twin pregnancies

Children (n) Monochorionic Dichorionic
220 205
Uncomplicated TTS sIUGR Uncomplicated sIUGR
190 14 ⁎ 16 ⁎ 195 ⁎ 10
NICU 23/190 (13%) 6/14 (43%) 0.007 12/16 (75%) 0.001 22/195 (11%) 2/10 (20%)
Morbidity
Neurological 1/190 (0.5%) 3/14 (21%) 0.001 3/16 (19%) 0.001 1/195 (0.5%) 0
Periventricular leukomalacia 0 0 0 0 0
Intraventricular hemorrhage 1/190 (0.5%) 2/14 (14%) 0.013 2/16 (12%) 0.016 1/195 (0.5%) 0
Cerebral Infarction 0 1/14 (7%) 0.069 0 0 0
Respiratory 17/190 (9%) 6/14 (43%) 0.002 8/16 (50%) 0.001 15/195 (8%) 1/10 (10%)
Mechanical ventilation 7/190 (4%) 5/14 (36%) 0.001 6/16 (38%) 0.001 8/195 (4%) 1/10 (10%)
Bronchopulmonary dysplasia 3/190 (2%) 2/14 (14%) 0.039 3/16 (19%) 0.007 0 0 0
Gastrointestinal 6/190 (3%) 1/14 (7%) 0.397 2/16 (12%) 0.120 3/195 (1%) 1/10 (10%)
Necrotizing enterocolitis 2/190 (1%) 1/14 (7%) 0.193 2/16 (12%) 0.031 2/195 (1%) 1/10 (10%)
Cardiovascular 6/190 (3%) 4/14 (29%) 0.002 4/16 (27%) 0.004 5/195 (2%) 1/10 (10%)
Persistent ductus arteriosus 1/190 (0.5%) 3/14 (29%) 0.001 2/16 (12%) 0.016 0 0
⁎P value as compared to uncomplicated MC, calculated by Chi squared. NICU = need of neonatal intensive care unit.
102
around 3%. The accumulated risk of fetal death after 32 weeks
in these studies and the present one would then be 1.8% (8
deaths in 446 wins). Thus, it seems plausible that monochor-
ionicity increases the risk of intrauterine death, perhaps due
to the existence of acute inter-twin transfusion phenomena.
However, with intensive follow-up, as conducted in the above
studies, this increment appears to be very low or marginal
after 32 weeks. Whether a policy of elective preterm delivery
at 32 weeks might reduce this risk remains an open question.
As expected, the incidence of neonatal complications
was higher in MC pregnancies, particularly in those com-
plicated with TTS and sIUGR. Although the numbers are
small in this study, twins with sIUGR had a higher incidence
of respiratory and neurological complications in MC than in
DC pregnancies. These findings are in agreement with
recent reports suggesting that IUGR in MC twins is asso-
ciated with a higher incidence of neurological damage
[6,7,16]. The incidence of neurological complications may
be related to the existence of hemodynamic accidents
associated with acute feto-fetal transfusion episodes, which
could be more frequent and/or more deleterious in cases
with marked growth discordance.
Acknowledgments
This work was supported by grants from the European
Commission (Grant QLG1-CT-2002-01632) and the Fondo de
Investigación Sanitaria (Grant FIS02/0738).
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