Original Paper

Fetal Diagn Ther Received: September 14, 2018

Accepted after revision: December 13, 2018
DOI: 10.1159/000496204 Published online: February 14, 2019

The Significance of Yolk Sac Number in

Monoamniotic Twins
Christine Fenton a Karen Reidy b, c Marina Demyanenko a
     

Ricardo Palma-Dias b–d Stephen Cole e Mark P. Umstad d, e

     

a Department
of Obstetrics and Gynaecology, The Royal Women’s Hospital, Parkville, VIC, Australia;
b Pauline
Gandel Imaging Centre, The Royal Women’s Hospital, Parkville, VIC, Australia; c Pregnancy Research Centre,
 

Department of Maternal Fetal Medicine, The Royal Women’s Hospital, Parkville, VIC, Australia; d The University of
 

Melbourne, Department of Obstetrics and Gynaecology, The Royal Women’s Hospital, Parkville, VIC, Australia;
e Department of Maternal Fetal Medicine, The Royal Women’s Hospital, Parkville, VIC, Australia
 

Keywords
Monoamniotic twins · Yolk sac · Twin pregnancy · Adverse
pregnancy outcome · First trimester ultrasound
Abstract
Background: Detection of a single yolk sac on early first tri-
mester ultrasound was previously thought to be a reliable
diagnostic feature of monochorionic monoamniotic (MCMA)
twin pregnancies. Objectives: To determine the frequency
of two yolk sacs in MCMA twin pregnancies and the associa-
tion of yolk sac number with pregnancy outcomes. Meth-
ods: A retrospective cohort analysis of MCMA twins man-
aged at a tertiary obstetric centre from January 2003 until
February 2017. All MCMA twin pregnancies were diagnosed
on tertiary centre ultrasound and, where possible, placental
histopathology postnatally. All MCMA twin pregnancies, in-
cluding conjoined twins, with available first trimester ultra-
sounds from 5 to 11 weeks’ gestation were included in the
analysis. MCMA pregnancies without available first trimester
ultrasounds and triplet pregnancies which included a MCMA
pair were excluded from the study. Results: Sixty-seven
MCMA cases were identified over 14 years. Thirty-eight cases
were included in the analysis. There was one yolk sac identi-
fied in 26 cases (68%) and two yolk sacs in 12 cases (32%).
Two yolk sacs were associated with a higher proportion of
male fetuses (33%, 4 out of 12, vs. 8%, 2 out of 26; p = 0.01).
There were no other significant differences between one
and two yolk sacs for maternal or neonatal outcomes. Con-
clusions: Two yolk sacs are present in up to a third of all
MCMA twin pregnancies, dispelling the original concept
that a single yolk sac is diagnostic of MCMA pregnancies.
Yolk sac number should not be used to determine amnionic-
ity. The presence of two yolk sacs on first trimester ultra-
sound is associated with an increased rate of male fetuses.
The number of yolk sacs has no other significant impact on
perinatal outcomes. © 2019 S. Karger AG, Basel
Introduction
Monochorionic monoamniotic (MCMA) twins are
thought to result from separation of a single cell mass at
days 8–12 following fertilization and are characterized by
a single chorionic and amniotic sac [1]. These pregnan-
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© 2019 S. Karger AG, Basel Christine Fenton

Department of Obstetrics and Gynaecology, The Royal Women’s Hospital
20 Flemington Road
Washington University

E-Mail karger@karger.com
Parkville, VIC 3052 (Australia)
www.karger.com/fdt
Downloaded by:

E-Mail christine.fenton @ thewomens.org.au

cies carry a high risk of adverse pregnancy outcomes in-
cluding perinatal death, preterm delivery, and an in-
creased incidence of congenital abnormalities. Major an-
atomical anomalies are seen in up to 26% of all MCMA
pregnancies [2]. Accurate diagnosis of amnionicity is im-
perative to advise prognosis and guide management de­
cisions including the degree of surveillance required.
Exclusion of monoamnionicity prevents excessive moni-
toring and unnecessary interventions associated with in-
correct diagnosis.
Ultrasound diagnosis of MCMA twin pregnancies re-
quire findings of an absent intertwin membrane, best de-
tected after 8 weeks’ gestation on transvaginal ultrasound
[3–5]. During the second trimester, the presence of cord
entanglement is pathognomonic of monoamnionicity
[1]. The detection of a single yolk sac on early first trimes-
ter ultrasound was previously thought to reliably diag-
nose MCMA pregnancies [3, 6, 7]; however, this concept
has now been challenged with case studies described of
MCMA twin pregnancies in which two yolk sacs have
been detected [4, 8–11].
Yolk sacs are an important imaging feature in all early
pregnancies. Detection of a yolk sac is crucial in diagnos-
ing a true intrauterine gestational sac, and an absent yolk
sac is always associated with a poor pregnancy outcome
[12]. Abnormal yolk sacs, in particular those with larger
diameters, are associated with increased frequency of
miscarriage and preterm birth [13–17]. In embryonic de-
velopment, yolk sacs are an essential component, provid-
ing nutritional, metabolic, and haemopoetic functions, as
well as contributing to the early fetal gastrointestinal sys-
tem [18]. Reaching its highest level of function at 4–7
weeks’ gestation, the yolk sac increases in size until 10
weeks, thereafter gradually diminishing in size, and it is
not detectable on ultrasound from approximately 13
weeks’ gestation [12].
The objective of this study is to determine the inci-
dence of two yolk sacs in MCMA twins and the associa-
tion of yolk sac number with adverse pregnancy out-
comes.
Materials and Methods
Study Design and Participants
This was a retrospective cohort analysis of all MCMA twins
managed at the Royal Women’s Hospital, Melbourne, Australia,
from January 2003 until February 2017. Approval for the conduct
of this retrospective audit study was obtained from our institu-
tion’s Human Research Ethics Committee. Hospital clinical and
ultrasound databases were used to identify MCMA pregnancies
during this period. All MCMA twin pregnancies were diagnosed
2 Fetal Diagn Ther
DOI: 10.1159/000496204
on tertiary centre ultrasound findings of a single placenta and an
absent intertwin amniotic membrane. Where possible, amnionic-
ity was confirmed by placental histopathological analysis postna-
tally. Histopathological confirmation was not possible in cases of
early miscarriage and termination of pregnancy.
All MCMA twin pregnancies, including conjoined twins, with
available first trimester ultrasounds from 5 to 11 weeks’ gestation
were included in the analysis. Triplet pregnancies which included
a MCMA pair were excluded from the study. Ultrasound scans
were either performed at our hospital’s tertiary ultrasound service
or by external imaging providers. Final confirmation of yolk sac
number was determined by a single experienced obstetric ultra-
sound specialist on review of images. Where it was not possible to
obtain direct images from external providers, specific mention of
yolk sac number on ultrasound reports was deemed sufficient. We
excluded all MCMA twin pregnancies without an early first tri-
mester ultrasound, pregnancies where ultrasound images were un-
able to be obtained, and pregnancies that did not have specific
mention of yolk sac number on the ultrasound report. Perinatal
outcomes were determined from the hospital medical records and
hospital electronic clinical information systems. The following
perinatal data were collected: maternal age at pregnancy outcome,
gravida, parity, mode of conception, pregnancy outcomes, fetal ab-
normalities, gestational age at pregnancy outcome, delivery mode,
common maternal conditions of pregnancy (gestational diabetes
and pregnancy-induced hypertension), antenatal admission days,
sex of fetus, birth weight, Apgar scores, days admitted to neonatal
intensive or special care unit, respiratory distress syndrome, and
intubation.
All cases of MCMA twin pregnancies surviving to 26 weeks’
gestation were admitted from this time until delivery in accor-
dance with local hospital protocols. Routine cardiotocography was
performed for at least 1 h, three times daily. Prophylactic beta-
methasone was administered between 26 and 28 weeks’ gestation,
and repeat doses of betamethasone were administered in accor-
dance with the Antenatal Corticosteroid Clinical Practice Guide-
lines Panel (Auckland, New Zealand) [19]. Delivery was planned
by caesarean section at 32 weeks’ gestation.
Statistical Analysis
GraphPad Prism (version 6.00 for Mac; GraphPad Software, La
Jolla, CA, USA) was used to generate statistical analyses. The
Mann-Whitney test was used for non-parametric data comparing
the two unpaired groups; and for parametric data, an unpaired t
test was used. The χ2 (Fisher’s exact) test was used to compare
pregnancy outcomes, Apgar scores, fetal abnormalities, rates of
intrauterine growth retardation, and sex of fetuses. A p value of
<0.05 was used to determine statistical significance.
Results
Sixty-seven cases of MCMA twin pregnancies were
identified over the 14-year period. Thirty-eight cases
were included in the analysis; 26 cases (68%) with one
yolk sac and 12 (32%) with two yolk sacs identified on first
trimester ultrasound (Fig.  1). Figures 2 and 3 display
MCMA twins within our series with one and two yolk
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 67 MCMA twins
identified

29 MCMA twins excluded

– No early 1st trimester
ultrasound (19)
– Unable to locate
1st trimester ultrasound
images (10)

38 MCMA twins
included in
analysis

26 (68%) with one yolk 12 (32%) with two yolk

sac on 1st trimester sacs on 1st trimester
ultrasound ultrasound

Fig. 1. Flowchart of monochorionic monoamniotic (MCMA) twin

pregnancy participants. Fig. 2. Transabdominal ultrasound image at 9+ weeks showing a
single gestational sac containing two embryos and a single yolk sac.

sacs detected on early first trimester ultrasound, respec-

tively. The overall maternal characteristics were compa-
rable between these two groups in terms of age, parity,
and mode of conception (Table 1).
Pregnancies with one yolk sac seen on first trimester
ultrasound had a 62% (16 of 26) rate of both babies being
live born compared with 42% (5 of 12) both live born in
the group with two yolk sacs (p = 0.46). There were simi-
lar rates of miscarriage in both groups with 20% (5 of 26)
in the one-yolk-sac group as compared to 25% (3 of 12)
in the two-yolk-sacs group. All miscarriages resulted in
the demise of both twins. There were 4 terminations of
pregnancy in the one-yolk-sac group (16%) and 3 in the
two-yolk-sacs group (25%). In the one-yolk-sac group,
there was one case of a miscarriage of one twin at 7 weeks’
gestation with subsequent delivery of a liveborn singleton Fig. 3. Transvaginal ultrasound image at 6+ weeks showing a single
at 39 weeks’ gestation, while in the two-yolk-sacs group, intrauterine gestational sac containing 2 yolk sacs (2 live embryos
there was one case of selective fetal reduction for anen- present, not shown in this image).
cephaly which resulted in miscarriage of the remaining
twin.
Pregnancies affected by fetal abnormalities, including
acardiac and conjoined twins, were comparable between diac rotation), 3 conjoined twins, 1 acardiac twin, 1 exom-
the groups (19%, 5 out of 26, vs. 33%, 4 out of 12, p = 0.42). phalos, and 1 anencephaly. Excluding conjoined twins, all
Overall, 9 of the 38 pregnancies had a congenital anoma- twins with a fetal abnormality were part of a discordant
ly detected: 2 cardiac anomalies (transposition of the anomalous twin pairing. There were 2 conjoined twins in
great arteries, severe pulmonary stenosis), 1 respiratory the one-yolk-sac group and 1 conjoined twin in the two-
anomaly (left lung agenesis with significant leftward car- yolk-sacs group, all cases of which were either terminated
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Yolk Sacs in Monoamniotic Twins Fetal Diagn Ther 3

DOI: 10.1159/000496204
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 Table 1. Maternal characteristics

Characteristics One yolk sac Two yolk sacs Overall p value

(n = 26) (n = 12) (n = 38)

Mean maternal age ± SD, years 29.9±5.5 28.9±7.3 29.6±6.0 0.23

Multiparous, n (%) 15 (58) 6 (50) 21 (55) 0.73
ART, n (%) 4 (15) 1 (8) 5 (13) 0.66

SD, standard deviation; ART, assisted reproductive techniques.

Table 2. MCMA twin pregnancy outcomes based on yolk sac number in pregnancies resulting in two live births

Outcomes One yolk sac Two yolk sacs Overall p value

(n = 16) (n = 5) (n = 21)

Mean gestation at delivery ± SD, weeks 30.9±1.8 32.3±2.1 31.2±1.8 0.74

Pregnancy-induced hypertension, n 0 0 0 –
Gestational diabetes mellitus, n (%) 5 (31) 0 5 (24) 0.28
Unplanned caesarean section, n (%) 8 (50) 1 (20) 9 (43) 0.24
Mean antenatal admission ± SD, days 34.5±16 36.2±22 34.9±18 0.51

MCMA, monochorionic monoamniotic; SD, standard deviation.

Table 3. Neonatal outcomes for the 21 MCMA pregnancies resulting in two live births

Outcomes One yolk sac Two yolk sacs Overall p value

(n = 32 neonates) (n = 10 neonates) (n = 42 neonates)

Birth weight, g 1,619±327 1,522±419 1,597±346 0.68

Birth weight <10th centilea 7 (22) 5 (50) 12 (29) 0.12
Apgar at 1 min <7 13 (42; of 31) 10 (70) 20 (49; of 41) 0.16
Apgar at 5 min <7 1 (3; of 31) 1 (10) 2 (5; of 41) 0.43
Stay in NICU, days 44.1±22 37.9±11 42.6±20 0.32
Respiratory distress syndrome 21 (66) 7 (70) 28 (67) 0.99
Intubation 11 (50) 3 (30) 14 (33) 0.80
30 days survival 32 (100) 10 (100) 42 (100) –

Values are presented as mean ± SD or n (%). MCMA, monochorionic monoamniotic; SD, standard deviation;
NICU, neonatal intensive care unit. a Based on growth charts by Hadlock et al. [26].

at the parents’ request or miscarried during the first tri-
mester.
There was a higher proportion of pregnancies with fe-
male fetuses (50%, 19 of 38) compared to male fetuses
(16%, 6 of 38) in all pregnancies. There were 13 cases
(34%) in which fetal sex could not be determined due to
early gestation at demise. In the two-yolk-sacs group,
there was a statistically significant higher proportion of
pregnancies with male fetuses with 4 of 12 (33%) com-
pared to 2 of 26 (8%) in the one-yolk-sac group (p = 0.01).
All pregnancies with both fetuses surviving to 17
weeks’ gestation (n = 21) continued to result in two live
births after 28 weeks’ gestation, with a mean gestational
age at birth of 31 weeks’ gestation. All pregnancies were
delivered by caesarean section. Fifty-seven percent (12 of
21) had planned caesarean sections at 32–33 weeks’ gesta-
tion, while 43% (9 of 21) underwent unplanned caesarean
sections at 27–32 weeks’ gestation. The indications for the
9 unplanned caesarean sections were: abnormal cardioto-
cography (3), preterm labour (2), twin anaemia polycy-
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thaemia sequence (2), critically abnormal Dopplers (1),
and preterm prelabour rupture of the membranes (1).
There were no significant differences in gestational age at
birth or rate of unplanned caesarean sections based on
yolk sac number (Table 2). There were also no significant
differences in neonatal outcomes between the one- and
two-yolk-sacs groups (Table 3).
Placental histopathology was available for 62% (16 of
26) and 50% (6 of 12) of pregnancies with one and two
yolk sacs, respectively. For all pregnancies resulting in
two live births, placental histopathology was available for
95% (20 of 21). In all cases examined, placental histopa-
thology confirmed the ultrasound diagnosis of monoam-
nionicity.
Discussion and Conclusion
Yolk Sac Number in MCMA Twins
To our knowledge, this is the largest cohort of MCMA
twins reporting on yolk sac number. Our study has shown
two yolk sacs to be present in 32% of all MCMA twin
pregnancies studied. This dispels the original concept
that a single yolk sac is a diagnostic feature of MCMA
pregnancies.
Yolk sacs differentiate in close temporal proximity to
that of the amniotic cavity. This led to the premise that,
in twin pregnancies, amnionicity could be accurately es-
tablished by the number of yolk sacs seen on first trimes-
ter ultrasound. With yolk sacs being the first detectable
feature of an intrauterine pregnancy, this could allow for
earlier diagnosis of MCMA twin pregnancies prior to ex-
clusion of an intertwin membrane, which is possible
from approximately 8 weeks’ gestation on transvaginal
ultrasound. Early studies with this theory were small [3,
6, 7] with only 6 total cases of MCMA pregnancies in-
cluded.
In 2006, Shen et al. [4] were the first to refute the am-
nion number equaling yolk sac number hypothesis, re-
porting on 3 cases of monochorionic diamniotic (MCDA)
twins with only a single yolk sac seen. However, they con-
cluded that the presence of two yolk sacs would still reli-
ably predict diamnionicity [4].
Since 2010, several cases of MCMA twins with two
yolk sacs emerged with six reported in the literature [8–
11, 20]. None of these examples described formal histo-
pathological confirmation of amnionicity, with two cases
confirmed on gross examination of the membranes and
placenta postnatally, while the other four had no docu-
mented examination of the placentae. In one of these
Yolk Sacs in Monoamniotic Twins
studies, by Murakoshi et al. [9], it was suggested that cas-
es of MCMA pregnancies with two yolk sacs could in fact
be MCDA pregnancies with spontaneous rupture of the
dividing membrane or creation of an incomplete dividing
membrane. No evidence of a dividing membrane was
seen on either ultrasound or histological examination in
our series.
In 2017, a study by Park et al. [21] reported on an ad-
ditional 4 cases of 11 MCMA twin pregnancies (36%)
with two yolk sacs seen on first trimester ultrasound. This
is in accordance with the incidence detected in our cur-
rent study, where 32% (12 of 38) of all MCMA twin preg-
nancies had two yolk sacs. With the addition of our study
to the existing literature, there are now 22 documented
cases of MCMA twins in which two yolk sacs were de-
tected.
Yolk Sac Number as Predictor of Pregnancy Outcome
In our series, the presence of two yolk sacs on first tri-
mester ultrasound was associated with an increased rate
of pregnancies with male fetuses. Yolk sac number was
not associated with any other significant differences in
pregnancy characteristics or perinatal outcomes.
Within this study, the sex ratio (the proportion of
males to the combination of males and females) was 0.24
amongst all of the MCMA twins, which is in accordance
with the known predominance of female fetuses among
MCMA twin pregnancies [22]. The preponderance of
male fetuses in the two-yolk-sacs group is an interesting
finding. Although this finding probably reflects the small
number of cases, it is interesting to consider whether it is
indicative of the timing of cleavage. Given that MCDA
twins, when cleavage likely occurs at days 3–8, have a sex
ratio of 0.484, and conjoined twins, with cleavage not
having occurred by day 13, have a sex ratio of 0.230 [23,
24], we considered that the presence of two yolk sacs sug-
gests cleavage closer to day 8 and an increased likelihood
of male fetuses. On the contrary, the presence of a single
yolk sac suggests a later cleavage and more likelihood of
female fetuses. The susceptibility of females to monozy-
gotic twinning has been postulated to be a consequence
of X-inactivation with the potential for the developing
cells to act aneuploid with a subsequent slowing of devel-
opment [22]. This delayed development may lead to the
missing of critically timed events and the increase in con-
genital anomalies seen in these twins [22, 25]. It is impor-
tant to highlight that the presumed timings of cleavage,
and indeed the entire concept of cleavage as opposed to
fusion, remain unproven and the subject of ongoing de-
bate [1].
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Fetal Diagn Ther 5
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 Due to the dependence of the embryo on the yolk sac
for development, and as most major anatomical abnor-
malities arise during embryonic development [26], we
had hypothesized that an increased yolk sac number
could be associated with a reduction in anatomical abnor-
malities. This reduction was not observed in our series.
The strengths of our study include this being the larg-
est cohort of MCMA twins in which yolk sac number has
been investigated. In addition, all MCMA twins were
managed at a single centre with a standardized approach
to the management of MCMA pregnancies, limiting vari-
ation between clinical practice and standards of care.
The major limitation of this analysis is the small sam-
ple size despite this being the largest case series from a
single institution of which we are aware. This is inevitable
in any single-centre study involving MCMA twins. Fur-
ther analysis with multiple collaborating centres or the
development of a register of MCMA twins is needed.
Other limitations include the retrospective nature of the
study and, subsequently, the high exclusion rate. Forty-
three percent (29 of 67) of all identified cases were ex-
cluded due to an inability to access first trimester ultra-
sound images or lack of an early first trimester scan in
which yolk sac number could be reliably identified. With
a large percentage of cases excluded with an unknown
number of yolk sacs, this may have affected the accuracy
of our overall proportions of one and two yolk sacs in
MCMA twin pregnancies.
Incomplete histopathological confirmation of all
MCMA twin pregnancies is a limitation of the study.
However, the percentage of available placental histopa-
thology was comparable between pregnancies with one
and two yolk sacs, with 62 and 50% available, respective-
ly. The majority of unavailable histopathology was from
cases of miscarriage and termination. Placental histopa-
thology was available for 95% of all live MCMA births (20
of 21).
Another potential limitation is the variation in report-
ing of first trimester ultrasounds. Whenever possible, a
single experienced obstetric ultrasound specialist re-
viewed the ultrasound images. This was not possible in
cases when external ultrasound images were unable to be
obtained. In these cases, specific mention of yolk sac
number on the report by the radiologist was deemed suf-
ficient; however, we are unable to ascertain the accuracy
of reporting. There are also some cases in which yolk sac
number was determined at a later stage (10–11 weeks’
gestation). This raised the possibility that two yolk sacs
may have been missed due to earlier regression of one
yolk sac or incomplete visualization of both yolk sacs.
6 Fetal Diagn Ther
DOI: 10.1159/000496204
Two yolk sacs are common in MCMA twin pregnan-
cies, dispelling the original concept that yolk sac number
should equal amnion number. Yolk sac number should
no longer be relied upon as an early marker in determin-
ing amnionicity on first trimester ultrasound. Diagnosis
should be delayed until the accurate exclusion of the in-
tertwin membrane from 8 weeks’ gestation on transvagi-
nal ultrasound. Larger cohort or multicentre studies are
required to determine the true significance of yolk sac
number on pregnancy outcomes for MCMA twins.
Statement of Ethics
Approval for the conduct of this retrospective audit study was
obtained from our institution’s Human Research Ethics Commit-
tee (The Royal Women’s Hospital, Melbourne, Australia). The au-
thors have no ethical conflicts to disclose.
Disclosure Statement
The authors have no conflicts of interest to declare.
Funding Sources
N/A.
Author Contributions
All authors were involved in the drafting of the manuscript. All
provided approval of the version to be published and agree to be
accountable for all aspects of the work. In addition to this, all au-
thors further contributed in the undertaking of the study. C.F. con-
tributed to acquisition, analysis, and interpretation of data. K.R.
identified cases. M.D. contributed to acquisition of data. R.P.-D.
was involved in interpreting ultrasounds of cases and provided
substantial contributions to the design of the work. S.C. was in-
volved in the design and conception of the work. M.P.U. provided
substantial contributions to the design and conception of the work.
References  1 McNamara HC, Kane SC, Craig JM, Short
RV, Umstad MP. A review of the mechanisms
and evidence for typical and atypical twin-
ning. Am J Obstet Gynecol. 2016 Feb;214(2):
172–91.
  2 Roqué H, Gillen-Goldstein J, Funai E, Young
BK, Lockwood CJ. Perinatal outcomes in
monoamniotic gestations. J Matern Fetal
Neonatal Med. 2003 Jun;13(6):414–21.
  3 Bromley B, Benacerraf B. Using the number
of yolk sacs to determine amnionicity in early
first trimester monochorionic twins. J Ultra-
sound Med. 1995 Jun;14(6):415–9.
128.252.67.66 - 2/18/2019 10:44:34 AM
Fenton/Reidy/Demyanenko/Palma-Dias/
Cole/Umstad
Washington University
Downloaded by:
  4 Shen O, Samueloff A, Beller U, Rabinowitz R.
Number of yolk sacs does not predict amni-
onicity in early first-trimester monochorionic
multiple gestations. Ultrasound Obstet Gyne-
col. 2006 Jan;27(1):53–5.
 5 Bora SA, Papageorghiou AT, Bottomley C,
Kirk E, Bourne T. Reliability of transvaginal
ultrasonography at 7-9 weeks’ gestation in the
determination of chorionicity and amnionic-
ity in twin pregnancies. Ultrasound Obstet
Gynecol. 2008 Oct;32(5):618–21.
  6 Monteagudo A, Timor-Tritsch IE, Sharma S.
Early and simple determination of chorionic
and amniotic type in multifetal gestations in
the first fourteen weeks by high-frequency
transvaginal ultrasonography. Am J Obstet
Gynecol. 1994 Mar;170(3):824–9.
  7 Levi CS, Lyons EA, Dashefsky SM, Lindsay
DJ, Holt SC. Yolk sac number, size and mor-
phologic features in a monochorionic mono-
amniotic twin pregnancy. Can Assoc Radiol J.
1996 Apr;47(2):98–100.
  8 Lu J, Cheng YK, Ting YH, Law KM, Leung
TY. Pitfalls in assessing chorioamnionicity:
novel observations and literature review. Am
J Obstet Gynecol. 2018 Sep;219(3):242–54.
  9 Murakoshi T, Ishii K, Matsushita M, Shinno
T, Naruse H, Torii Y. Monochorionic mono-
amniotic twin pregnancies with two yolk sacs
may not be a rare finding: a report of two cas-
es. Ultrasound Obstet Gynecol. 2010 Sep;
36(3):384–6.
10 Bishop DK. Yolk-sac number in monoamni-
otic twins. Obstet Gynecol. 2010 Aug; 116(2
Suppl 2):504–7.
Yolk Sacs in Monoamniotic Twins
11 Corbett SL, Shmorgun D. Yolk sac number
does not predict reliably amnionicity in
monochorionic twin pregnancies: a case of a
monochorionic monoamniotic twin preg-
nancy with two distinct yolk sacs on early
first-trimester ultrasound. Ultrasound Obstet
Gynecol. 2012 May;39(5):607–8.
12 Tan S, Pektaş MK, Arslan H. Sonographic
evaluation of the yolk sac. J Ultrasound Med.
2012 Jan;31(1):87–95.
13 Tan S, Gülden Tangal N, Kanat-Pektas M, Si-
rin Özcan A, Levent Keskin H, Akgündüz G,
et al. Abnormal sonographic appearances of
the yolk sac: which can be associated with ad-
verse perinatal outcome? Med Ultrason. 2014
Mar;16(1):15–20.
14 Lindsay DJ, Lovett IS, Lyons EA, Levi CS,
Zheng XH, Holt SC, et al. Yolk sac diameter
and shape at endovaginal US: predictors of
pregnancy outcome in the first trimester. Ra-
diology. 1992 Apr;183(1):115–8.
15 Küçük T, Duru NK, Yenen MC, Dede M,
Ergün A, Başer I. Yolk sac size and shape as
predictors of poor pregnancy outcome. J Per-
inat Med. 1999;27(4):316–20.
16 Cho FN, Chen SN, Tai MH, Yang TL. The
quality and size of yolk sac in early pregnancy
loss. Aust N Z J Obstet Gynaecol. 2006 Oct;
46(5):413–8.
17 Berdahl DM, Blaine J, Van Voorhis B, Dokras
A. Detection of enlarged yolk sac on early ul-
trasound is associated with adverse pregnan-
cy outcomes. Fertil Steril. 2010 Sep; 94(4):
1535–7.
18 Sadler T. Langman’s Medical Embryology.
12th ed. Baltimore: MD Lippincott Willams &
Wilkins; 2012.
Fetal Diagn Ther
DOI: 10.1159/000496204
19 Antenatal Corticosteroid Clinical Practice
Guidelines Panel. Antenatal corticosteroids
given to women prior to birth to improve fe-
tal, infant, child and adult health: clinical
practice guidelines. 2015. Auckland; Liggins
Institute, The University of Auckland; 2015.
20 Meller C, Wojakowski A, Izbizky G, Aiello H,
Otaño L. Number of yolk sacs in the diagnosis
of monoamnionicity. J Ultrasound Med. 2014
Jun;33(6):1091–7.
21 Park SY, Chung JH, Han YJ, Lee SW, Kim
MY. Prediction of Amnionicity Using the
Number of Yolk Sacs in Monochorionic Mul-
tifetal Pregnancy. J Korean Med Sci. 2017
Dec;32(12):2016–20.
22 Hall JG. Twinning. Lancet. 2003 Aug;
362(9385):735–43.
23 James WH. Sex ratio and placentation in
twins. Ann Hum Biol. 1980 May-Jun; 7(3):
273–6.
24 Derom C, Vlietinck R, Derom R, Van den
Berghe H, Thiery M. Population-based study
of sex proportion in monoamniotic twins. N
Engl J Med. 1988 Jul;319(2):119–20.
25 Lubinsky MS, Hall JG. Genomic imprinting,
monozygous twinning, and X inactivation.
Lancet. 1991 May;337(8752):1288.
26 O’Rahilly R, Müller F. Developmental stages
in human embryos: revised and new measure-
ments. Cells Tissues Organs. 2010;192(2):73–
84.
27 Hadlock FP, Harrist RB, Martinez-Poyer J. In
utero analysis of fetal growth: a sonographic
weight standard. Radiology. 1991 Oct;181(1):
129–33.
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