MRI of Fetal and Maternal Diseases in Pregnancy 1st ed.

12. MR Imaging of Multiple Gestations

Monika Bekiesinska-Figatowska 

(1)

Department of Diagnostic Imaging, Institute of Mother and Child, Warsaw, Poland

Monika Bekiesinska-Figatowska

Email: m.figatowska@mp.pl

Keywords

Magnetic resonance imaging (MRI)Twin pregnancy

12.1 Introduction

The phenomenon of twinning has always attracted attention and twins have been considered as extraordinary from the beginning of history. For example, in Greek mythology, the gods Apollo and Artemis have been twins; in Roman mythology, twin brothers, Romulus and Remus, have founded Rome. One of the oldest images of twins in America dates back to approximately 200 B.C. and comes from Guatemala: it is a sculpture representing the Maya Hero Twins. In Christian tradition, the twins Cosmas and Damian, physicians and martyrs, have become saints and patrons of medicine.

The number of multifetal pregnancies increases with the increasing maternal age (which by itself causes increased incidence of fertility-inhibiting conditions) and the increasing rate of ovulation induction and assisted reproduction – these phenomena are observed more and more frequently in our aging societies. When assisted reproduction technology (ART) is used, the overall twin rate is approximately 26 % – ART has been associated with 30-fold increase in multiple pregnancies. The probability of having at least one fetus with a chromosomal abnormality in multifetal pregnancy is higher than in a singleton pregnancy of the same age – the rates in the literature are various, but in general, it is thought that there are 1.5–3 times more defects per fetus in twin pregnancy.

With the increasing age of pregnant women and the increasing number of conceptions achieved with use of ART, there is an increasing need for prenatal diagnosis and especially for noninvasive diagnostic techniques, including diagnostic imaging techniques.

With the advent of ultrasound (US) in the second half of the twentieth century, we began to image twins in utero, and the first images of twins acquired with magnetic resonance imaging (MRI) were published in 1988 [1], not a long time after the first publication concerning fetal MRI in general which appeared in 1983.

12.2 General Considerations About Multiple Gestations

Twins can either be monozygotic (“identical”), which means that they develop from one zygote that splits into two embryos, or dizygotic (“fraternal”) – developing from two eggs fertilized by two separate sperm cells. With natural conception, the majority of twins are dizygotic (DZ). There is significantly increased trend in monozygotic (MZ) twinning after ART. Dizygotic twins are always dichorionic (DC). They form when splitting takes place by the third day after fertilization. Monozygotic twins may be dichorionic or monochorionic (MC). MC twins may be diamniotic (DA) – they occur when the split takes place between days 4 and 8 after fertilization, or monoamniotic (MA) – when splitting occurs after day 9 after fertilization. MCMA twins are very rare – only 2 % of MC twins are MA. If one thinks of MC twinning as of an embryonic accident (an embryo that was supposed to be a singleton becomes twins), one realizes that two embryos fight for the same territory which is a single placenta [2]. MC twins are at high risk for adverse outcome due to complications related to placental vascular anastomoses. Arteriovenous anastomoses result in twin-twin transfusion syndrome (TTTS), twin anemia-polycythemia syndrome (TAPS), growth discordance, and arterio-arterial anastomoses – in twin reversed-arterial-perfusion syndrome (TRAPS). That is why it is chorionicity that determines fetal outcome in twin pregnancies [3] with monochorionic monozygosity being the greatest exposure to anomalies and death [4] – Sect. 12.6.

It is obvious that DZ twins may have discordant anomalies as they have different DNA. MZ twins are expected to have the same abnormalities, if any, because they have identical DNA sequences. Pre-twinning mutations concern both twins indeed, but also post-twinning mutations may occur after splitting of the fertilized egg and then only one of the MZ twins is affected by the resulting disease – that is why MZ twins also may have discordant anomalies in as many as 20 % of cases. Anencephaly and congenital heart anomalies are found most often in these MCMA twins which are discordant.

Fetal growth disturbances detected as, e.g., crown-rump length (CRL) discordance in the twins on the first trimester ultrasound mean that one of the twins is at risk of structural abnormalities or chromosomal aneuploidy. If CRL discordance is bigger than 10 %, there is a 25 % chance of congenital abnormalities in twin pregnancy. CRL discordance of 20 % and more as well as nuchal translucency of 3 mm and more increase the probability of structural abnormalities in one twin by six times [5]. The parents should be informed about the need for increased frequency of US scanning and most likely for MR imaging in these cases. Precise diagnosis is crucial for the choice of management of discordant anomalous twins. MRI more and more often becomes necessary for counseling parents on treatment options and possible outcomes.

12.3 Technical Considerations About MRI of Multiple Gestations

The same well-known factors that make sonographic assessment of a single fetus difficult apply to multiple pregnancy as well; the additional factor is that in twin pregnancy, one fetus may interfere with the attempt to evaluate another one on ultrasound which is not a problem for MRI (Fig. 12.1). When ultrasound is difficult, better images may be obtained by MRI; when US is equivocal and inconclusive, MRI may be a problem-solving technique (Fig. 12.2), that is why MRI is used as an adjunct to ultrasound in the prenatal diagnosis, also in multiple pregnancies. Like Arabin cervical pessary to noninvasively prevent preterm birth in twin pregnancies with short cervix, MRI becomes necessary to noninvasively assess the fetuses in multifetal pregnancies.

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Fig. 12.1

Thick slab magnetic resonance imaging (MRI). Sonographic assessment of the head of the left twin is difficult due to his position and the position of the right twin who covers his head. This difficulty can be overcome on MRI

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Fig. 12.2

Twenty-one gestational weeks. Thick slab MRI (a) shows why the assessment of the back of the left twin is difficult for the sonographer. In SSFSE sequence, T2WI, axial plane, one can clearly see the meningocele (MC) in the lumbar-sacral part of the vertebral column (b) and features of Chiari II malformation in the posterior cranial fossa (c)

Search for the existing literature in PubMed does not bring any results as far as triplet and higher number multiple pregnancies are concerned in terms of the use of MRI to assess the fetuses. The author’s personal experience also concerns only twin pregnancies, and these will be the subject of further considerations.

The sequences of MR examination are exactly the same when imaging a twin pregnancy. There is one major technical problem in this case, i.e., that it is more time consuming: first, because there are two fetuses to be examined and evaluated and secondly, because twins are much more mobile than singletons, especially in earlier gestation (Fig. 12.3), and this makes imaging more difficult and longer [6]. The time of the study cannot be too long as it is uncomfortable for the mother, so imaging twins is a challenge to radiologists and radiographers.

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Fig. 12.3

Twin pregnancy examined at 21 gestational weeks in SSFSE sequence, T2WI (ab). Note the artifacts resulting from movement of the fetuses and of the amniotic fluid (white and black fluid). The contents of the (en)cephalocele sac are difficult to assess. Second fetal MRI (SSFSE/T2WI) at the gestational age of 33 weeks with significantly reduced movements and artifacts (ce) and postnatal imaging (f – FSE/T2WI, g – SE/T1WI post Gad) allows diagnosis of atretic cephalocele containing the meninges, fibrous tissue, and – possibly – some altered brain tissue

12.4 Developmental Anatomical Differences Between Singletons and Multiples

Twins are not the same as two single fetuses – for example, it has been shown in the study of cortical folding that the normal development of the brains of twins differs from that in singleton pregnancies. The cortical thickness, surface, and volume are significantly reduced at birth in twins as compared to singletons [7]. The entire volume of cerebrospinal fluid is greater in twins than in singletons, while the ventricle volumes do not differ between these two groups [8]. The cortical maturation and gyrification are delayed in twins, and the same applies to body maturation [7], e.g., twins are usually underweight for dates. Abdominal circumference is decreased in twins as compared to singletons [9]. This has to be taken into consideration when interpreting the findings and comparing them to the existing atlases or other sources of normal images and measurements’ values.

At the same time, general maturation of fetuses in multiple pregnancies in terms of neurological performance can be accelerated by 3–4 weeks or even more in small for gestational age (SGA) twins as compared to the appropriately grown infants of the same gestational age. The accelerated brain and lung maturation reflects an adaptation of the fetus to early extrauterine life [10]. Therefore, even “term” means something else in case of multiples as compared to singletons – it occurs earlier in twins who are ready to be born earlier; they do not grow any more after 38th gestational week while singletons do [11].

12.5 Congenital Anomalies Unrelated to Plurality

Congenital malformations occur more frequently in multifetal gestations because of the larger number of fetuses and the increased risk of anomalies in monozygotic pregnancies. But also, one fetus of a dizygotic twin pregnancy is twice more likely to have a chromosomal abnormality than a single one [412].

In general, irrespective of zygosity, chorionicity, and amnionicity, in most cases of twin pregnancies (80–90 %), only one fetus has a defect, but in 10–20 %, both babies are affected (Fig. 12.4) [3]. The latter concerns mainly monozygotic twins that have the same karyotype except for these situations when genetic discordance is observed. Certain abnormalities occur more frequently in monozygotic twins, and they include anencephaly, holoprosencephaly, hydrocephalus, sacrococcygeal teratoma, and cardiac anomalies [3912]. Esophageal atresia has been described as more common in twin pregnancies as well [9].

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Fig. 12.4

SSFSE sequence, T2WI, axial plane. Axial section through the pelvis of both fetuses is shown in one slice, and spinal dysraphism and myelomeningocele (MMC) can be diagnosed in both twins

Any congenital malformation seen in a singleton pregnancy can occur in multiple gestation, and its imaging characteristics are the same as described in the previous chapters (Fig. 12.5). Few available publications show that in a significant number of cases, MRI brings important new diagnostic information compared with ultrasound also in multifetal gestations (Fig. 12.6) [61314].

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Fig. 12.5

Fetal MRI in SSFSE sequence, T2WI. In the parasagittal-oblique section through the left twin, gastroschisis was found with herniation of the bowel. Below, one can see a rounded tissue mass (a) which – in view of bladder non-visualization in any sequence and projection – corresponds to bladder exstrophy (b)

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Fig. 12.6

In this pair of twins examined at the gestational age of 30 weeks, hydronephrosis and megaureter on the right side and no left kidney were found on US in one fetus. MRI (SSFSE, T2WI) disclosed the ectopic left kidney located between the bladder and the vertebral column in the right twin and confirmed the other findings (a – axial plane, b – coronal plane).

The correct diagnosis influences strongly the management which is somewhat different than in singleton pregnancies – the parents are offered three options:

1.

2.

3.

It is important to know the chorionicity (Sect. 12.6) before offering the third option because of the increased risk of loss of the unaffected fetus in monochorionic gestation.

In most countries, pregnancy termination is allowed up to approximately 24 weeks of gestation, so early diagnosis is necessary to elect this option. If the abnormalities occur or are detected later, there is still place to limit intensive care in neonatal clinic after birth which also requires psychological preparation of the parents.

Selective feticide is also subject to the risk of neurological complications: long-term outcome after selective termination of the affected fetus in MC pregnancy includes neurodevelopmental impairment in 5 % and cerebral palsy in 2 % of cases. It is advisable then to image the surviving fetus after the procedure like after sIUFD (Sect. 12.6.1).

12.6 Complications of Twin Gestations

As stated before, monozygosity carries higher malformation risk, but it is chorionicity that is the main determinant of fetal outcome in twin pregnancies [3] with monochorionic monozygosity as the greatest exposure to anomalies and death [4]. Therefore, it is crucial to know the chorionicity as soon as possible, and it is US that is capable of determining chorionicity and amnionicity and of differentiating mono- and dichorionic twin pregnancies in the first trimester, optimally around the 10th week of gestation, on the basis of:

·               The presence of chorion between the amniotic membranes forming a thick septum in dichorionic diamniotic pregnancy, known as a “Y” sign, a lambda sign, or a twin peak sign

·               Two amniotic sacs in monochorionic diamniotic pregnancy with a thin intertwin membrane perpendicular to the placenta (a “T” sign)

·               One placenta, lack of membrane between the fetuses, very close cord insertions, or an enlarged cord in monochorionic monoamniotic pregnancy [312]

Knowing the chorionicity, one can explain the difference in size of the twins: in dichorionic twins, intrauterine growth retardation (IUGR) of the smaller fetus can be diagnosed, while in monochorionic gestation, twin-twin transfusion syndrome (TTTS) should be taken into account (Sect. 12.6.2) although not every discordance in MC twins is TTTS: selective IUGR (sIUGR) should also be kept in mind.

Complications specific for twin gestations include consequences of intrauterine death of one twin to another one, twin-twin transfusion syndrome (TTTS), twin anemia-polycythemia syndrome (TAPS), twin reversed-arterial-perfusion syndrome (TRAPS), and conjoined twinning.

12.6.1 Intrauterine Death of One Twin

Single intrauterine fetal demise (sIUFD) is described here although it should not be considered as a complication specific for twin gestations in every case because it may result from the same problems that cause intrauterine fetal demise in a singleton pregnancy, i.e., structural abnormalities, abruption, placental insufficiency, growth restriction, cord abnormalities, infection, and maternal disease. It is estimated to occur in up to 7 % of twin gestations in the second and third trimester. According to some authors, in more than 20 % of twin pregnancies, first trimester embryonic loss (vanishing twin syndrome) occurs up to 7 weeks of gestation [16].

In DC pregnancy, vanishing twin syndrome is the most frequent complication and may be considered as spontaneous reduction of multiple pregnancy. The vanishing twin is then partially or completely reabsorbed by the co-twin. If the process of fetal resorption fails, the dead fetus is compressed by its growing co-twin to a flattened form called fetus papyraceus which may be seen on imaging (US, MRI) in the second half of pregnancy. In rare cases, it may block the cervix and require a cesarean section to deliver the living co-twin.

In dichorionic pregnancy, the surviving twin is usually normal – its impairment occurs in 1 % of cases. The outcome is significantly worse in case of a survivor in the monochorionic pregnancy with the impairment rate of 18 %. Damage to the central nervous system, gastrointestinal system, kidneys, and lungs is observed in many of these cases [9]. Both ultrasound and MRI were recommended to be performed 3–4 weeks after the death of one twin in order to detect anomalies in the survivor [17]. Nowadays, this delay is not justified anymore – with use of diffusion-weighted imaging (DWI), acute cerebral insult can be detected much earlier: as early as even after 24 h [18].

Co-twin death occurs in approximately 4 % of cases of DC pregnancies and 12 % of MC ones [17].

12.6.2 Twin-Twin Transfusion Syndrome (TTTS)

TTTS occurs in approximately 10 % of MC twins and is defined as severe amniotic fluid discordance.

The syndrome is staged according to Quintero score which may be used for both US and MRI:

·               Stage I: Oligohydramnios around the donor and polyhydramnios around the recipient.

·               Stage II: Stage I + the bladder in the donor is not identifiable.

·               Stage III: Stages I and II + abnormal blood flow in the umbilical cords of the twins (abnormal Doppler ultrasound findings in umbilical artery, umbilical vein, as well as in medial cerebral artery).

·               Stage IV: Stage I, II, and III + fetal hydrops in the recipient.

·               Stage V: Stages I, II, III, and IV + one or both twins’ death (usually the donor dies first) [19] (Fig. 12.7a).

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Fig. 12.7

(ac). SSFSE/T2WI. At the gestational age of 22 weeks, TTTS stage V was diagnosed (a) and abnormal cortical folding in the survivor was suspected (bc). FSE/T2WI. This finding was confirmed in the neonatal MRI – abnormal cortical folding with polymicrogyria was shown (de)

The features of blood flow cannot be shown on MRI, and such data is missing from MR examinations, but the remaining features can be assessed by both methods. In both examinations, polyuria in the recipient is supported by bladder distention, and an MRI study has shown renal pelvic distention in more than 50 % of recipients as well as cardiomegaly, supporting cardiac dysfunction [20].

The death of one twin causes acute exsanguination through superficial placental anastomoses to the second twin. This may make the second twin die, or if not, about ¼ of the survivors suffer from severe neurodevelopmental impairment with multicystic brain lesions and brain atrophy.

Severe cerebral morbidity is acquired prenatally also in TTTS patients treated with fetoscopic laser surgery: 52 % vs. 17 % in controls (dichorionic twins) with hemorrhage and ischemia as the most often possible brain lesions [21]. This is a place for magnetic resonance imaging because prenatal ultrasound, even performed in tertiary centers, underestimates the risk even in 75 % of cases. Some authors suggest to perform fetal MRI one week after laser procedure [22]; the others stress the necessity to detect acute ischemia as early as possible: even after 24 h [23]. Not only the ischemic brain damage is important but also abnormal cortical folding in the ischemic region of the brain (Fig. 12.7b–e). Depending on the time of brain injury by TTTS, different forms of ischemic damage are observed. The time threshold is gestational age of 26–28 weeks. If the injury occurs before this age, we deal with hydranencephaly, callosal necrosis, porencephaly, polymicrogyria/heterotopia, ventriculomegaly with cerebral atrophy, and periventricular leukomalacia. If the injury occurs after this age, we observe ventriculomegaly with cerebral atrophy, periventricular leukomalacia, multicystic leukoencephalopathy, subcortical leukomalacia, lenticulostriate vasculopathy, and basal ganglia damage. Irrespective of gestational age, hemorrhagic injury may occur including germinal matrix hemorrhage, ventriculomegaly with clots, parenchymal hemorrhage, and diffuse hemorrhage [24]. The superiority of fetal MRI over sonography for visualizing many of these brain abnormalities has already been well documented – especially damage to the white matter and gray matter abnormalities is hardly detectable on ultrasound (Figs. 12.7 and 12.8) [25].

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Fig. 12.8

(ab). SSFSE/T2WI. In this pair of twins (29 gestational weeks), only ventriculomegaly was diagnosed on US in one of the twins, while MRI showed cystic lesion close to the ventricle in the same twin

TTTS may lead to functional and structural cardiac abnormalities, especially in a recipient twin. Hypervolemia in a recipient may cause biventricular hypertrophy and hyperplasia and ventricular hypokinesia. Increased heart size is due to hypertrophy and not to dilatation. The right ventricle is affected earlier than the left one. If TTTS is treated with amniodrainage, cardiovascular disease progresses. With laser coagulation therapy, which addresses pathophysiology, cardiovascular disease regresses. The hypovolemic donor twin is probably more likely to have coarctation of the aorta and/or hypoplastic aortic arch [26]. This is also a field for the further development of the evolving techniques of fetal cardiac MRI.

Fetal ischemic limb necrosis is also found in association with TTTS – amniotic band syndrome occurs in up to 3 % of twins with TTTS.

12.6.3 Twin Anemia-Polycythemia Syndrome (TAPS)

TAPS is a severe hemoglobin discordance. It occurs in approximately 5 % of previously uncomplicated MC pregnancies and in approximately 10 % of pregnancies after laser therapy for TTTS – due to persistent placental vascular anastomoses. In these cases, it can be considered as iatrogenic. In TAPS, there is no oligo-/polyhydramnios sequence, but there is a small anemic donor and a big polycythemic recipient twin. The syndrome leads to IUFD or brain damage, if undetected. The brain is typically injured by infarctions in the recipient and hemorrhages in the donor. About 8 % of babies with TAPS have severe cerebral injury. Besides TAPS causes the risk of cardiac failure and hydrops to the anemic twin and of ischemic limb lesions to the polycythemic twin.

Prenatal diagnosis of TAPS is based on Doppler measurements of peak systolic velocity in the middle cerebral artery with the evident difference between donor and recipient: increased values in the donor twin, suggestive of fetal anemia, and decreased in the recipient twin, suggestive of polycythemia.

The placenta shows also some characteristic features on US in TAPS: it is hyperechogenic and thick in a donor and hypoechogenic and thin in a recipient. These features are not included in the diagnostic criteria but are helpful in the diagnosis. The liver displays similar echogenicity: it is bright in a donor and black in a recipient on US. These features would be most likely reflected by signal intensity (SI) changes on MRI – deposits of iron in the liver of the recipient should probably cause decrease in SI which requires further studies.

Selective feticide is one of the treatment options for TAPS if one of the fetuses has brain damage. MRI is very helpful in these most difficult cases when the parents are offered this option because brain damage must be documented without any doubt.

12.6.4 Twin Reversed-Arterial-Perfusion Syndrome (TRAPS)

TRAPS occurs in approximately 1 % of MZ pregnancies. In this syndrome, there is an acardiac recipient suffering from varying degrees of hypoplasia, usually of the upper part of the body (with the most frequent variant of acardiac acephalus, lacking the head and upper limbs, with only rudimentary thoracic and abdominal organs) and a normal “pump” twin which provides circulation for its co-twin. Compensatory chamber hypertrophy is found in pump twin resulting in cardiomegaly and further on in ascites, hydrothorax, pericardial effusion, hepatomegaly, and polyhydramnios as signs of cardiac failure. Early diagnosis is necessary to perform umbilical cord occlusion in the acardiac twin thus preventing the pump twin from heart failure and death.

Pump twin is also at risk of ischemic brain injury which is best assessed by means of MRI [27]. MRI is also helpful in differentiating acardius amorphous – one of the forms of the acardiac twin – from intrauterine mass when ultrasound is inconclusive [28].

12.6.5 Conjoined Twinning

Conjoined twins are monochorionic monoamniotic ones. They form when a single fertilized oocyte splits incompletely between day 12 and 15 after fertilization (although it has also been proposed that conjoined twining may result from fusion of originally separate monovular embryos) and occur with the incidence of 1:30,000–1:100,000 gestations and 1:250,000 live births. Various types of conjoined twins have been described, and some kind of classification has been created depending on the site and extent of union [29], but each set of such twins is unique and has its own characteristics requiring detailed analysis. Eighty percent of conjoined twins have additional anomalies. Accurate diagnosis of shared organs and associated abnormalities is necessary to determine prognosis, for counseling and planning surgical separation: emergency or postponed [14]. It is not obvious in every case that termination of pregnancy is elected – for example, pyopagus (twins joined at lower spine and buttocks) or craniopagus (joined at any part of the skull except the face and foramen magnum) has good prognosis as no major organs are shared. In this second case, for example, MRI is the best method to assess the possibility of separation by ruling out cortical fusion between the brains (Fig. 12.9). Although the diagnosis of conjoined twins is usually sonographic, it may require MRI in later pregnancy or just to better show the spatial relationships of the abnormal and shared organs [30].

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Fig. 12.9

MCMA twins diagnosed as craniopagus on MRI. First MRI at the gestational age of 19 weeks: (a) SSFSE/T2WI, (b) DWI. The separate brains were confirmed on the second MRI, performed at 30 gestational weeks (c – FIESTA/2D). The separate brains were also confirmed on the postnatal MRI and angiography, and the girls were prepared for the surgical separation (the skin was cultured), but they died due to renal insufficiency

12.7 Psychological Aspects of Fetal MRI

The role of MRI is not only to confirm and further characterize the anomalies but also to exclude them if they are wrongly diagnosed or suspected by ultrasound. To rule out pathology is equally important as to diagnose it (Fig. 12.10). It is of utmost importance to the parents-to-be and has great impact on their psychological status, especially of the mother. This element of the role of prenatal MRI and of the radiologists’ work is not sufficiently emphasized in the literature [31]. In the available literature, mostly the anxiety associated with the examination is stressed: physical restraint, noise level, examination’s duration, and anxiety for the baby which is increased by the severity of the referral diagnosis [32]. But MRI, as the last noninvasive method in the diagnostic chain, can also relieve tension and reduce stress experienced by parents later in the pregnancy. In twin pregnancies, it is usually a question of ruling out pathology in the second twin when the first is known to have a congenital defect. In rare cases of conjoined twins, it is a question of showing the possibility of separation (Fig. 12.9).

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Fig. 12.10

SSFSE/T2WI of the 21-week twin pregnancy. Sonographically, hydrocephalus and cerebellar hypoplasia in one fetus and cerebellar hypoplasia in the second one were diagnosed. MRI confirmed the abnormalities in the first twin (ab) and showed normal cerebrum and cerebellum in the second one (c), thus freeing the parents from the fear of a second child

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