Surveillance of Monochorionic Twins

Monochorionic twins are a classification of twins that occur in monozygotic pregnancies. In these pregnancies, a single fertilized oocyte divides into two separate embryos after the third day of normal embryonic development [1]. Approximately 20% of twin pregnancies are monochorionic, and these twins often have significantly more complications than their dichorionic counterparts [2]. These complications can be potentially life threatening and are further discussed in this chapter. The complications occur because of the development of vascular anastomosis between the fetuses that can affect the fetal blood supply of either twin, leading to increased fetal morbidity and mortality [2-4]. For this reason, monochorionic pregnancies need more intense surveillance and management than single gestation and dichorionic pregnancies [3-4]. In this chapter, we will review dating, establishing chorionicity, complications and recommended surveillance of monochorionic pregnancies.

Although the guidelines suggest dating between 11 weeks and 13 weeks and 6 days, chorionicity can often be established as early as 8 weeks gestational age to correctly identify high risk pregnancies and promptly direct their care. Ideally, nuchal translucency should be measured when the crown-rump length (CRL) measures between 45 and 84 mm [4]. It is generally recommended that the dating estimate in twin pregnancies should be based on the larger of the two fetuses' crown-rump length (CRL). [4]. Some studies suggest using the CRL of the smaller fetus or calculating the mean CRL as they have been shown to be more accurate in both prospective and retrospective analyses [4-7]. However, the concern is that these two methods can lead providers into erroneously classifying the larger twin as large for gestational age (LGA) which can deceive them into falsely believing that the smaller twin is an adequate size [4]. This error could potentially have detrimental effects leading to missed surveillance and inadequate management of the pregnancy. When a woman presents after 14 weeks gestational age, the head circumference of the larger fetus should be used to date the pregnancy [4]. For pregnancies conceived by in-vitro fertilization (IVF) dating is based on the age of the embryo [4].

Chorionicity refers to the number of placentas identified in a pregnancy. The ideal time to establish chorionicity is early on in gestation, specifically it is most accurate before 13 + 6 weeks of gestation [4]. A retrospective study done by Lee et al of 410 twins found that establishing chorionicity by sonographic signs at or before 14 weeks gestational age demonstrated a good sensitivity (89.9%), specificity (99.5%), and positive and negative predictive value (97.8% and 97.5% respectively) [3,8]. If transvaginal or transabdominal ultrasound clearly demonstrates two placentas or fetal sex discordance, then the pregnancy is said to be dichorionic [3-4]. 
When only one distinct placenta is visualized, chorionicity is determined by ultrasound examination of the thickness of the amniotic membrane that inserts into the placenta between the two fetuses. In dichorionic diamniotic twins, there is a thick projection of this echogenic membrane that is at least three layers [3,4,8]. The layers consist of a fused chorion with a thin layer of amnion on both sides separating the two fetuses [3,4,8]. This is said to give the appearance of a “lambda” and is known as the “lambda or delta sign” [2-4]. Monochorionic diamniotic (MCDA) twins are only separated by the two thin layers of the amnion which is said to give the appearance of a “T” and is known as the “T-sign” and is less than 2 millimeters thick [2,4]. 
Measuring the number of placental masses is not a reliable method to determine chorionicity because dichorionic placentas can be next to each other and falsely appear as one placenta on ultrasound [4]. Additionally, a study that examined 109 monochorionic placentas found that 3% of them had two placental masses potentially leading to false interpretations of the pregnancy [4,9]. These patients had bipartite placentas that were proven to be monochorionic on macroscopic examination and demonstrated the classic “T-sign” on ultrasound [9]. Chorionicity of women who present after 14 weeks of gestation is evaluated by the same ultrasonographic signs described above, along with determining if there is discordance of fetal sex suggesting dizygotic twins [4]. It is crucial to refer all patients in whom chorionicity cannot be established to a tertiary center for comprehensive evaluation. These pregnancies carry a significant risk of maternal and fetal morbidity and mortality, necessitating specialized care and monitoring [4]. Pregnancies where chorionicity is unknown should be managed as monochorionic [4]. 
    When determining chorionicity it is also important to document if the fetuses share the same amniotic sac, known as amnionicity. If there is an absence of a membrane between the twins, they are deemed monochorionic monoamniotic (MCMA) twins [4]. However, the examiner must be cautious because it is possible to not visualize a membrane when imaging quality is poor, when the pregnancy is less than 8 weeks, when the amnion is not developed enough to be a specular reflector, or when there is a “stuck twin” in twin-to-twin transfusion syndrome. Other methods for determining amnionicity included looking for cord entanglement on color and pulsed-wave Doppler ultrasound [4]. In MCMA twins pulsed-wave Doppler demonstrates two different arterial waveforms and heart rates at the same sampling gate [4]. 

Multifetal gestations carry increased risk for stillbirth, fetal anomalies, preterm delivery, growth issues and short-term and long-term neonatal and infant morbidity [10-12]. Additionally, women with multifetal gestations are at an increased risk of gestational diabetes, anemia, hemorrhage, cesarean delivery, postpartum depression, and hypertensive disorders of pregnancy [3,13-19].
Monochorionic pregnancies have a higher risk of developing complications in pregnancy including fetal and congenital anomalies, prematurity, fetal growth restriction, and stillbirth [20-22]. Complications unique to monochorionic pregnancies include selective fetal growth restriction, twin-to-twin transfusion syndrome, twin anemia polycythemia sequence, and twin reversed arterial perfusion sequence [20,23-24]. Cord entanglement is a risk unique to MCMA pregnancies however studies have concluded that it does not contribute to prenatal morbidity and mortality [25,26]. Conjoined twins are a rare complication that exclusively arises in MCMA pregnancies. Additionally, MCMA twins are at an increased risk of intrauterine demise when compared to other twin types [4].

Fetal Anomalies
    The most common fetal anomalies in twin pregnancies include central nervous system, renal, and cardiac malformations [27]. The prevalence of congenital anomalies in monochorionic twins is nearly twice that of dichorionic twins [27]. Four congenital malformations associated with twinning are perimembranous ventricular septal defect (VSD), atrial septal defect (ASD) secundum type, hypoplastic left heart syndrome (HLHS), and omphalocele [28]. MCDA twins have a 7% chance of having one twin with a congenital heart defect (CHD) [29]. If one twin is affected, the risk of both twins having a CHD in a MCDA pregnancy is 26% [29]. The risk of CHD in MCMA twins is 57% [29]. For monochorionic pregnancies, there is increased concordance for the flow lesions including HLHS, congenital stenosis of aortic valve, coarctation of the aorta, and ostium secundum type ASD [30]. 

Selective Fetal Growth Restriction
    Selective fetal growth restriction (sFGR) occurs in 10-15% of monochorionic pregnancies. Selective fetal growth restriction is defined as a condition when one fetus has an estimated fetal weight (EFW) or abdominal circumference (AC) < 10th percentile and an intertwin discordance > 25th percentile [4]. Selective FGR is most commonly due to unequal sharing of the placental mass and vasculature in monochorionic twin pregnancies [31]. Other causes can include fetal anomalies and velamentous cord insertion. The definition of sFGR varies amongst clinicians and recommending societies. An intertwin discordance of 20% distinguishes pregnancies with an increased risk of adverse outcomes [4]. The American College of Obstetricians and Gynecologists considers discordant fetal growth to be a difference of 15 to 25% [3]. Other studies suggest an EFW discordance of 18% to be an accurate predictor for adverse outcomes [32]. 
    Screening and diagnosis for sFGR are established by calculation of EFW by measurement of the fetal head, abdomen, and femur length. EFW discordance is calculated by the following formula: (weight of larger twin – weight of smaller twin) × 100)/weight of larger twin [4]. However, it is important to consider that assessing EFW using ultrasound is less accurate in twin pregnancies compared to singleton pregnancies [33]. Once diagnosis is established, these twins should receive increased fetal surveillance, fetal Doppler studies, and delivery planning due to the significantly increased risk of perinatal loss [34,35]. 
Selective FGR in monochorionic twin pregnancies are further classified based on umbilical artery Doppler waveforms. In Type I, the umbilical artery Doppler waveform for the growth restricted fetus has continuous positive end-diastolic flow. For Type II, there is a persistently absent or reversed end-diastolic flow (AREDF). Type III is categorized by a cyclic or intermittent pattern of AREDF [4]. Type I has a high survival rate greater than 90%. Type II and type III have an increased risk of intrauterine demise (IUD) of the growth restricted twin. Type III is associated with a 10-20% risk of unpredictable sudden death of the growth restricted fetus. If IUD occurs due to sFGR, the surviving co-twin has an elevated risk of neurological damage [36,37]. Additionally, twins complicated by sFGR have an incidence of severe cerebral injury up to 10% [38]. Management of sFGR can include conservative management with early delivery, laser ablation, or cord occlusion of growth restricted fetus [4,39]. 

Twin-to-twin Transfusion Syndrome
    Twin-to-twin transfusion syndrome (TTTS) occurs in approximately 10-15% of MCDA pregnancies. It results from arteriovenous anastomoses in the monochorionic placenta. This leads to an imbalance in the fetal-placental circulation leading to one twin transfusing the other [40-43]. Diagnosis is made with ultrasonography indicating amniotic fluid imbalance. The donor twin will have oligohydramnios with a deepest vertical pocket (DVP) < 2cm and the recipient twin will have polyhydramnios with a DVP > 8cm. In the United States, a DVP > 8 cm is used as the polyhydramnios cut off throughout gestation. In Europe, polyhydramnios is defined as a DVP > 8 cm prior to 20 weeks gestation and DVP > 10 cm after 20 weeks gestation [44]. TTTS is staged with the Quintero Staging System which also considers ultrasound evaluation of the bladder, Dopplers of the umbilical artery, and evaluating for the presence of hydrops. Other classification systems that consider cardiac parameters of the donor and recipient twin have been proposed [44]. These include the CHOP-score, cardiovascular profile score, and Cincinnati score that consider different cardiac parameters including cardiothoracic ratio, ventricular wall thickness, atrioventricular regurgitation, myocardial performance index, and others [45-48]. Early diagnosis can allow for intervention with fetoscopic laser coagulation, amnioreduction, selective reduction by radiofrequency ablation or voluntary pregnancy termination [49,50]. If TTTS progresses and is left untreated, it can lead to fetal demise in up to 90% of cases [51,52].

Twin Anemia Polycythemia Sequence
    Twin anemia polycythemia sequence (TAPS) occurs in up to 5% of pregnancies and may be present in up to 13% of cases of TTTS following laser ablation [38]. It results from arteriovenous anastomoses allowing for slow transfusion of blood from donor to recipient twin. The antenatal diagnosis and staging are based on discordant middle cerebral arterial (MCA) Doppler peak systolic velocities, indicating anemia in the donor twin and polycythemia in the recipient twin [53]. The outcomes differ based on syndrome severity and gestational age of presentation but can lead to intrauterine demise and neurodevelopmental delay [54]. Management also varies based on severity but can include laser ablation or intrauterine blood or exchange transfusion [55]. A trial is currently underway to evaluate if fetoscopic laser therapy will improve neonatal outcome by prolonging the pregnancy [56].

Twin Reversed Arterial Perfusion Sequence
Twin reversed arterial perfusion sequence (TRAP) which may also be known as acardiac twin pregnancy occurs in 1% of monochorionic twins [57]. It results from perfusion of an acardiac twin by the normal twin who serves as the pump through arterioarterial anastomosis [58,59]. The pump twin can develop high-output cardiac failure [59]. Management varies from cord coagulation, cord ligation, photocoagulation of the anastomoses, and intrafetal laser therapy [60].

Conjoined Twins
    Conjoined twins occur in 1% of monochorionic twin pregnancies [61]. Ultrasound is used to establish the diagnosis. Many classifications exist including cephalopagus, pygopagus, cephalothoracopagus, and thoracopagus which is the most common [62]. The diagnosis is associated with significant morbidity and mortality. 

Due to the increased risk of complications with monochorionic twin pregnancies, there is an increased need for surveillance in order to detect potential abnormalities and guide management. Additionally, the early determination of chorionicity is important for proper patient counseling and guidance. Clinical practice guidelines suggest a first trimester scan followed by a scan every 2 weeks after 16 weeks for uncomplicated monochorionic twins [4].

11-14 weeks
    During the 11–14-week period patients should receive an initial ultrasound to establish dating, labeling of twins, and chorionicity to aid in proper surveillance, counseling, and pregnancy planning. First trimester ultrasound should also look for any major anomalies and measure nuchal translucency [63]. This is also the ideal time to consider screening for fetal chromosomal abnormalities including Trisomy 21 [4]. Multiple options are available for screening including the combined test and non-invasive prenatal testing [4]. Importantly, screening tests for chromosomal abnormalities are not as accurate for twin gestations as they are for singleton gestations [64]. There is a higher risk for inaccurate test results if a fetal demise, vanishing twin, or anomaly is identified in one fetus [3].

16-18 weeks
    In the 16–18-week period, fetal growth, deepest vertical pocket (DVP), and umbilical artery Doppler pulsatility index (UA-PI) should be recorded to assist in the early detection of TTTS and fetal growth restriction [4]. Screening should continue every 2 weeks thereafter if normal parameters are present [4]. If there is evidence of abnormal DVP, then weekly UA and middle cerebral artery (MCA) Dopplers are warranted [4]. Additionally, documentation of fetal bladder on ultrasound may be warranted to determine Quintero Staging of TTTS. 

20 weeks
Between 18-20 weeks, a detailed anatomy scan should be performed to screen for any evident anomalies including but not limited to neural tube defects, cardiac defects, gastrointestinal abnormalities, craniofacial defects, and brain abnormalities [63, 34]. Due to the increased risk of congenital heart disease, all monochorionic twins should receive a fetal echocardiogram by a skilled sonographer at 18-22 weeks gestation [65]. At the time of the anomaly scan during the second trimester, cervical length should also be measured to screen for preterm birth, with the cutoff being 25mm [4].
Serial growth ultrasounds with fetal biometry should continue to be performed every 2-4 weeks to screen for fetal growth restriction (FGR) [66]. Due to the concern of discordant growth and selective fetal growth restriction, discordance should be calculated and documented starting at 20 weeks [4]. Additionally, measurement of DVP and UA-PI should continue every 2 weeks to screen for TTTS and FGR. Starting at 20 weeks gestation, middle cerebral artery peak systolic volume (MCA-PSV) should be measured to screen for TAPS and every 2 weeks thereafter [4].
If sFGR is identified during screening, fetal growth should then be assessed at least every two weeks with biometry. The frequency of fetal Doppler with UA-PI and MCA-PSV should be increased to at least once a week. If UA Dopplers are abnormal, this may warrant measurement of the ductus venosus blood flow to further assess the severity. Management and delivery timing of twins with sFGR should be determined based on assessment of fetal well-being, interval growth, biophysical profile, gestational age and other factors [4]. 
If sFGR leads to intrauterine demise, there is increased risk of demise, preterm delivery, and neurodevelopmental impairment in the surviving co-twin [67-69]. The surviving co-twin should undergo assessment of fetal Doppler and fetal biometry every 2-4 weeks [4]. Additionally, the fetal brain should be imaged 4-6 weeks after the demise of a co-twin to look for evidence of cerebral damage[4]. This can be conducted with neurosonography or fetal MRI with findings that have been reported including infarctions, multicystic encephalopathy, cerebral atrophy, intraventricular hemorrhage, cortical necrosis, subdural hematoma, and others [70,71]. 

22-36 weeks
    From 22-36 weeks, fetal growth should continue to be monitored every 2-4 weeks [66]. DVP, UA-PI, and MCA-PSV should be performed every 2 weeks to continue monitoring for development of FGR, TTTS, and TAPS [4].
    For MCDA twins, antenatal testing (fetal cardiotocography or biophysical profile) should begin at 32 weeks [72-74]. For MCMA twins, antenatal testing should be individualized [75-77]. Many clinicians recommend early inpatient management with daily fetal surveillance starting between 24-28 weeks. Frequency of surveillance while inpatient is individualized, and optimal management of these patients remains uncertain [75-77]. The timing of delivery for uncomplicated MCDA twins is 36 weeks and mode of delivery depends on twin presentation [3]. MCMA twins should deliver between 32-34 weeks by cesarean section to avoid cord complications [75-77]. 

In conclusion, multifetal gestations carry increased risk for fetal and maternal morbidity. Monochorionic twins have a higher risk of developing several complications and have their own unique complications including TTTS, TAPS, TRAP sequence, sFGR and conjoined twins. Hence, early determination of chorionicity during pregnancy is vital to identify individuals at high risk and provide appropriate counseling and referrals to Maternal Fetal Medicine. This allows for timely intervention and management of potential complications associated with specific chorionicity types, ensuring the best possible outcomes for these patients. Surveillance includes measurement of fetal growth, DVP, UA-PI, MCA-PSV, detailed anatomy scans, cervical length measurement, and fetal echocardiogram. Standardized monitoring intervals have been established but may vary based on case presentation and concern for specific complication. Early detection and intervention for TTTS and TAPS results in decreased morbidity and mortality. Therefore, it is extremely important that patients receive frequent surveillance throughout their pregnancy.

1.    Hall JG. Twinning. Lancet. 2003;362(9385):735-743. doi:10.1016/S0140-6736(03)14237-7
2.    Lu J, Cheng YKY, Ting YH, Law KM, Leung TY. Pitfalls in assessing chorioamnionicity: novel observations and literature review [published correction appears in Am J Obstet Gynecol. 2019 May;220(5):499]. Am J Obstet Gynecol. 2018;219(3):242-254. doi: 10.1016/j.ajog.2018.02.010
3.    American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins—Obstetrics, Society for Maternal-Fetal Medicine. Multifetal Gestations: Twin, Triplet, and Higher-Order Multifetal Pregnancies: ACOG Practice Bulletin, Number 231. Obstet Gynecol. 2021;137(6): e145-e162. doi:10.1097/AOG.0000000000004397
4.    Khalil A, Rodgers M, Baschat A, et al. ISUOG Practice Guidelines: role of ultrasound in twin pregnancy [published correction appears in Ultrasound Obstet Gynecol. 2018 Jul;52(1):140]. Ultrasound Obstet Gynecol. 2016;47(2):247-263. doi:10.1002/uog.15821
5.    Chaudhuri K, Su LL, Wong PC, et al. Determination of gestational age in twin pregnancy: Which fetal crown-rump length should be used? J Obstet Gynaecol Res. 2013;39(4):761-765. doi:10.1111/j.1447-0756.2012. 02054.x
6.    Dias T, Mahsud-Dornan S, Thilaganathan B, Papageorghiou A, Bhide A. First-trimester ultrasound dating of twin pregnancy: are singleton charts reliable? BJOG. 2010;117(8):979-984. doi:10.1111/j.1471-0528.2010. 02592.x
7.    Salomon LJ, Cavicchioni O, Bernard JP, Duyme M, Ville Y. Growth discrepancy in twins in the first trimester of pregnancy. Ultrasound Obstet Gynecol. 2005;26(5):512-516. doi:10.1002/uog.1966
8.    Lee YM, Cleary-Goldman J, Thaker HM, Simpson LL. Antenatal sonographic prediction of twin chorionicity. Am J Obstet Gynecol. 2006;195(3):863-867. doi: 10.1016/j.ajog.2006.06.039
9.    Lopriore E, Sueters M, Middeldorp JM, Klumper F, Oepkes D, Vandenbussche FP. Twin pregnancies with two separate placental masses can still be monochorionic and have vascular anastomoses. Am J Obstet Gynecol. 2006;194(3):804-808. doi: 10.1016/j.ajog.2005.09.015
10.    Scher AI, Petterson B, Blair E, Ellenberg JH, Grether JK, Haan E, Reddihough DS, Yeargin-Allsopp M, Nelson KB. The risk of mortality or cerebral palsy in twins: a collaborative population-based study. Pediatr Res. 2002 Nov;52(5):671-81. doi: 10.1203/00006450-200211000-00011. 
11.    Martin JA, Hamilton BE, Ventura SJ, Osterman MJ, Kirmeyer S, Mathews TJ, Wilson EC. Births: final data for 2009. Natl Vital Stat Rep. 2011 Nov 3;60(1):1-70.
12.    Rettwitz-Volk W, Tran TM, Veldman A. Cerebral morbidity in preterm twins. J Matern Fetal Neonatal Med. 2003 Apr;13(4):218-23. doi: 10.1080/jmf.13.4.218.223.
13.    Sivan E, Maman E, Homko CJ, Lipitz S, Cohen S, Schiff E. Impact of fetal reduction on the incidence of gestational diabetes. Obstet Gynecol. 2002 Jan;99(1):91-4. doi: 10.1016/s0029-7844(01)01661-1.
14.    Schwartz DB, Daoud Y, Zazula P, Goyert G, Bronsteen R, Wright D, Copes J. Gestational diabetes mellitus: metabolic and blood glucose parameters in singleton versus twin pregnancies. Am J Obstet Gynecol. 1999 Oct;181(4):912-4. doi: 10.1016/s0002-9378(99)70324-8. 
15.    Sibai BM, Hauth J, Caritis S, Lindheimer MD, MacPherson C, Klebanoff M, VanDorsten JP, Landon M, Miodovnik M, Paul R, Meis P, Thurnau G, Dombrowski M, Roberts J, McNellis D. Hypertensive disorders in twin versus singleton gestations. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. Am J Obstet Gynecol. 2000 Apr;182(4):938-42. doi: 10.1016/s0002-9378(00)70350-4.
16.    Luke B, Brown MB. Contemporary risks of maternal morbidity and adverse outcomes with increasing maternal age and plurality. Fertil Steril. 2007 Aug;88(2):283-93. doi: 10.1016/j.fertnstert.2006.11.008. 
17.    Conde-Agudelo A, Belizán JM, Lindmark G. Maternal morbidity and mortality associated with multiple gestations. Obstet Gynecol. 2000 Jun;95(6 Pt 1):899-904.
18.    Sheard C, Cox S, Oates M, Ndukwe G, Glazebrook C. Impact of a multiple, IVF birth on post-partum mental health: a composite analysis. Hum Reprod. 2007 Jul;22(7):2058-65. doi: 10.1093/humrep/dem123.
19.    Bailit JL. Hyperemesis gravidarium: Epidemiologic findings from a large cohort. Am J Obstet Gynecol. 2005 Sep;193(3 Pt 1):811-4. doi: 10.1016/j.ajog.2005.02.132. 
20.    Danon D, Sekar R, Hack KEA, Fisk NM. Increased stillbirth in uncomplicated monochorionic twin pregnancies: a systematic review and meta-analysis. Obstet Gynecol. 2013 Jun;121(6):1318-1326. doi: 10.1097/AOG.0b013e318292766b.
21.    Geipel A, Berg C, Katalinic A, Plath H, Hansmann M, Germer U, Gembruch U. Prenatal diagnosis and obstetric outcomes in triplet pregnancies in relation to chorionicity. BJOG. 2005 May;112(5):554-8. doi: 10.1111/j.1471-0528.2005.00627. x.
22.    Glinianaia SV, Obeysekera MA, Sturgiss S, Bell R. Stillbirth and neonatal mortality in monochorionic and dichorionic twins: a population-based study. Hum Reprod. 2011 Sep;26(9):2549-57. doi: 10.1093/humrep/der213.
23.    Søgaard K, Skibsted L, Brocks V. Acardiac twins: pathophysiology, diagnosis, outcome and treatment. Six cases and review of the literature. Fetal Diagn Ther. 1999 Jan-Feb;14(1):53-9. doi: 10.1159/000020889. 
24.    Mutchinick OM, Luna-Muñoz L, Amar E, Bakker MK, Clementi M, Cocchi G, da Graça Dutra M, Feldkamp ML, Landau D, Leoncini E, Li Z, Lowry B, Marengo LK, Martínez-Frías ML, Mastroiacovo P, Métneki J, Morgan M, Pierini A, Rissman A, Ritvanen A, Scarano G, Siffel C, Szabova E, Arteaga-Vázquez J. Conjoined twins: a worldwide collaborative epidemiological study of the International Clearinghouse for Birth Defects Surveillance and Research. Am J Med Genet C Semin Med Genet. 2011 Nov 15;157C (4):274-87. doi: 10.1002/ajmg.c.30321. 
25.    Dias T, Mahsud-Dornan S, Bhide A, Papageorghiou AT, Thilaganathan B. Cord entanglement and perinatal outcome in monoamniotic twin pregnancies. Ultrasound Obstet Gynecol. 2010 Feb;35(2):201-4. doi: 10.1002/uog.7501.
26.    Rossi AC, Prefumo F. Impact of cord entanglement on perinatal outcome of monoamniotic twins: a systematic review of the literature. Ultrasound Obstet Gynecol. 2013 Feb;41(2):131-5. doi: 10.1002/uog.12345. 
27.    Glinianaia SV, Rankin J, Wright C. Congenital anomalies in twins: a register-based study. Hum Reprod. 2008 Jun;23(6):1306-11. doi: 10.1093/humrep/den104. Epub 2008 Apr 2. PMID: 18387962.
28.    Dawson AL, Tinker SC, Jamieson DJ, Hobbs CA, Berry RJ, Rasmussen SA, Anderka M, Keppler-Noreuil KM, Lin AE, Reefhuis J; National Birth Defects Prevention Study. Twinning and major birth defects, National Birth Defects Prevention Study, 1997-2007. J Epidemiol Community Health. 2016 Nov;70(11):1114-1121. doi: 10.1136/jech-2015-206302. 
29.    Manning N, Archer N. A study to determine the incidence of structural congenital heart disease in monochorionic twins. Prenat Diagn. 2006 Nov;26(11):1062-4. doi: 10.1002/pd.1556. 
30.    Hardin J, Carmichael SL, Selvin S, Lammer EJ, Shaw GM. Increased prevalence of cardiovascular defects among 56,709 California twin pairs. Am J Med Genet A. 2009 May;149A (5):877-86. doi: 10.1002/ajmg.a.32745. 
31.    Lewi L, Gucciardo L, Huber A, Jani J, Van Mieghem T, Done E, Cannie M, Grataco ́SE, Diemert A, Hecher K, Lewi P, Deprest J. Clinical outcome and placental characteristics of monochorionic diamniotic twin pairs with early- and late-onset discordant growth. Am J Obstet Gynecol 2008; 199: 511.e1 – 7. doi: 10.1016/j.ajog.2008.04.022.
32.    Breathnach F, McAuliffe F, Geary M, Daly S, Higgins J, Dornan J, Morrison JJ, Burke G, Higgins S, Dicker P, Manning F, Mahony R, Malone FD; Perinatal Ireland Research Consortium. Definition of intertwin birth weight discordance. Obstet Gynecol 2011; 118: 94 – 103. doi: 10.1097/AOG.0b013e31821fd208.
33.    Khalil A, D’Antonio F, Dias T, Cooper D, Thilaganathan B; Southwest Thames Obstetric Research Collaborative (STORK). Ultrasound estimation of birth weight in twin pregnancy: comparison of biometry algorithms in the STORK multiple pregnancy cohort. Ultrasound Obstet Gynecol 2014; 44: 210 – 220. doi: 10.1002/uog.13253.
34.    National Collaborating Centre for Women's and Children's Health (UK). Multiple Pregnancy: The Management of Twin and Triplet Pregnancies in the Antenatal Period. London: RCOG Press; 2011.
35.    D’Antonio F, Khalil A, Dias T, Thilaganathan B; Southwest Thames Obstetric Research Collaborative (STORK). Weight discordance and perinatal mortality in twins: analysis of the Southwest Thames Obstetric Research Collaborative (STORK) multiple pregnancy cohort. Ultrasound Obstet Gynecol 2013; 41: 643 – 648. doi: 10.1002/uog.12412. 
36.    Valsky DV, Eixarch E, Martinez JM, Crispi F, Grataco ́s E. Selective intrauterine growth restriction in monochorionic twins: pathophysiology, diagnostic approach and management dilemmas. Semin Fetal Neonatal Med 2010; 15: 342 – 348.
37.    Gratacos E, Carreras E, Becker J, Lewi L, Enrıquez G, Perapoch J, Higueras T, Cabero L, Deprest J. Prevalence of neurological damage in monochorionic twins with selective intrauterine growth restriction and intermittent absent or reversed end-diastolic umbilical artery flow. Ultrasound Obstet Gynecol 2004; 24: 159 – 163. doi: 10.1002/uog.1105. 
38.    Inklaar MJ, van Klink JM, Stolk TT, van Zwet EW, Oepkes D, Lopriore E. Cerebral injury in monochorionic twins with selective intrauterine growth restriction: a systematic review. Prenat Diagn 2014; 34: 205 – 213. 
39.    Chalouhi GE, Marangoni MA, Quibel T, Deloison B, Benzina N, Essaoui M, Al Ibrahim A, Stirnemann JJ, Salomon LJ, Ville Y. Active management of selective intrauterine growth restriction with abnormal Doppler in monochorionic diamniotic twin pregnancies diagnosed in the second trimester of pregnancy. Prenat Diagn 2013; 33: 109 – 115. 
40.    Emery SP, Bahtiyar MO, Dashe JS, Wilkins-Haug LE, Johnson A, Paek BW, Moon-Grady AJ, Skupski DW, O'Brien BM, Harman CR, Simpson LL. The North American Fetal Therapy Network Consensus Statement: prenatal management of uncomplicated monochorionic gestations. Obstet Gynecol. 2015 May;125(5):1236-1243. doi: 10.1097/AOG.0000000000000723. 
41.    Sueters M, Middeldorp JM, Lopriore E, Oepkes D, Kanhai HH, Vandenbussche FP. Timely diagnosis of twin-to-twin transfusion syndrome in monochorionic twin pregnancies by biweekly sonography combined with patient instruction to report onset of symptoms. Ultrasound Obstet Gynecol. 2006 Oct;28(5):659-64. doi: 10.1002/uog.3819.
42.    Royal College of Obstetricians and Gynaecologists . Consensus views arising from the 50th Study Group: multiple pregnancy. London: RCOG; 2006. Available at: http://www.rcog.org.uk/files/rcogcorp/uploadedfiles/StudyGroupConsensusViewsMultiplePregnancy.pdf . Retrieved June 19th, 2023.
43.    Lewi L, Gucciardo L, Van Mieghem T, de Koninck P, Beck V, Medek H, Van Schoubroeck D, Devlieger R, De Catte L, Deprest J. Monochorionic diamniotic twin pregnancies: natural history and risk stratification. Fetal Diagn Ther. 2010;27(3):121-33. doi: 10.1159/000313300. 
44.    Van Mieghem T, Lewi L, Gucciardo L, Dekoninck P, Van Schoubroeck D, Devlieger R, Deprest J. The Fetal Heart in Twin-to-Twin Transfusion Syndrome. Int J Pediatr. 2010:379792. doi: 10.1155/2010/379792. 
45.    Rychik J, Tian Z, Bebbington M, et al. The twin-twin transfusion syndrome: spectrum of cardiovascular abnormality and development of a cardiovascular score to assess severity of disease. American Journal of Obstetrics and Gynecology. 2007;197(4): 392.e1–392.e8. doi: 10.1016/j.ajog.2007.06.055.
46.    Shah AD, Border WL, Crombleholme TM, Michelfelder EC. Initial fetal cardiovascular profile score predicts recipient twin outcome in twin-twin transfusion syndrome. Journal of the American Society of Echocardiography. 2008;21(10):1105–1108. doi: 10.1016/j.echo.2008.05.004.
47.    Habli M, Michelfelder E, Livingston J, et al. Acute effects of selective fetoscopic laser photocoagulation on recipient cardiac function in twin-twin transfusion syndrome. American Journal of Obstetrics and Gynecology. 2008;199(4): 412.e1–412.e6. doi: 10.1016/j.ajog.2008.06.067. 
48.    Stirnemann JJ, Mougeot M, Proulx F, et al. Profiling fetal cardiac function in twin-twin transfusion syndrome. Ultrasound in Obstetrics and Gynecology. 2010;35(1):19–27. doi: 10.1002/uog.7488.
49.    Simpson LL. Twin-twin transfusion syndrome. Society for Maternal-Fetal Medicine [published erratum appears in Am J Obstet Gynecol 2013; 208:392]. Am J Obstet Gynecol 2013; 208:3–18. 
50.    Stamilio DM, Fraser WD, Moore TR. Twin-twin transfusion syndrome: an ethics-based and evidence-based argument for clinical research. Am J Obstet Gynecol. 2010 Jul;203(1):3-16. doi: 10.1016/j.ajog.2009.12.006.
51.    Roberts D, Neilson JP, Kilby MD, Gates S. Interventions for the treatment of twin-twin transfusion syndrome. Cochrane Database Syst Rev. 2014 Jan 30;(1):CD002073. doi: 10.1002/14651858.CD002073.pub3.
52.    Robyr R, Lewi L, Salomon LJ, Yamamoto M, Bernard JP, Deprest J, Ville Y. Prevalence and management of late fetal complications following successful selective laser coagulation of chorionic plate anastomoses in twin-to-twin transfusion syndrome. Am J Obstet Gynecol. 2006 Mar;194(3):796-803. doi: 10.1016/j.ajog.2005.08.069.
53.    Slaghekke F, Kist WJ, Oepkes D, Pasman SA, Middeldorp JM, Klumper FJ, Walther FJ, Vandenbussche FP, Lopriore E. Twin anemia-polycythemia sequence: diagnostic criteria, classification, perinatal management and outcome. Fetal Diagn Ther. 2010;27(4):181-90. doi: 10.1159/000304512.
54.    Slaghekke F, van Klink JM, Koopman HM, Middeldorp JM, Oepkes D, Lopriore E. Neurodevelopmental outcome in twin anemia-polycythemia sequence after laser surgery for twin-twin transfusion syndrome. Ultrasound Obstet Gynecol. 2014 Sep;44(3):316-21. doi: 10.1002/uog.13387. 
55.    Genova L, Slaghekke F, Klumper FJ, Middeldorp JM, Steggerda SJ, Oepkes D, Lopriore E. Management of twin anemia-polycythemia sequence using intrauterine blood transfusion for the donor and partial exchange transfusion for the recipient. Fetal Diagn Ther. 2013;34(2):121-6. doi: 10.1159/000346413.
56.    The TAPS Trial - Fetoscopic Laser Surgery for Twin Anemia-Polycythemia Sequence - a Multicenter Open-Label Randomized Controlled Trial. ClinicalTrials.gov identifier: NL6442700018. Updated June 16th, 2020. Accessed July 10th, 2023. https://clinicaltrials.gov/study/NCT04432168 
57.    Søgaard K, Skibsted L, Brocks V. Acardiac twins: pathophysiology, diagnosis, outcome and treatment. Six cases and review of the literature. Fetal Diagn Ther. 1999 Jan-Feb;14(1):53-9. doi: 10.1159/000020889. 
58.    Moore TR, Gale S, Benirschke K. Perinatal outcome of forty-nine pregnancies complicated by acardiac twinning. Am J Obstet Gynecol. 1990 Sep;163(3):907-12. doi: 10.1016/0002-9378(90)91094-s.
59.    Wong AE, Sepulveda W. Acardiac anomaly: current issues in prenatal assessment and treatment. Prenat Diagn. 2005 Sep;25(9):796-806. doi: 10.1002/pd.1269.
60.    Tan TY, Sepulveda W. Acardiac twin: a systematic review of minimally invasive treatment modalities. Ultrasound Obstet Gynecol. 2003 Oct;22(4):409-19. doi: 10.1002/uog.224. 
61.    Mutchinick OM, Luna-Muñoz L, Amar E, Bakker MK, Clementi M, Cocchi G, da Graça Dutra M, Feldkamp ML, Landau D, Leoncini E, Li Z, Lowry B, Marengo LK, Martínez-Frías ML, Mastroiacovo P, Métneki J, Morgan M, Pierini A, Rissman A, Ritvanen A, Scarano G, Siffel C, Szabova E, Arteaga-Vázquez J. Conjoined twins: a worldwide collaborative epidemiological study of the International Clearinghouse for Birth Defects Surveillance and Research. Am J Med Genet C Semin Med Genet. 2011 Nov 15;157C (4):274-87. doi: 10.1002/ajmg.c.30321.
62.    Baken L, Rousian M, Kompanje EJ, Koning AH, van der Spek PJ, Steegers EA, Exalto N. Diagnostic techniques and criteria for first trimester conjoined twin documentation: a review of the literature illustrated by three recent cases. Obstet Gynecol Surv. 2013 Nov;68(11):743-52. doi: 10.1097/OGX.0000000000000000.
63.    Salomon LJ, Alfirevic Z, Bilardo CM, Chalouhi GE, Ghi T, Kagan KO, Lau TK, Papageorghiou AT, Raine-Fenning NJ, Stirnemann J, Suresh S, Tabor A, Timor-Tritsch IE, Toi A, Yeo G. ISUOG practice guidelines: performance of first-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol. 2013 Jan;41(1):102-13. doi: 10.1002/uog.12342. Erratum in: Ultrasound Obstet Gynecol. 2013 Feb;41(2):240.
64.    American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins—Obstetrics; Committee on Genetics; Society for Maternal-Fetal Medicine. Screening for Fetal Chromosomal Abnormalities: ACOG Practice Bulletin, Number 226. Obstet Gynecol. 2020 Oct;136(4): e48-e69. doi: 10.1097/AOG.0000000000004084.
65.    Patient Safety and Quality Committee, Society for Maternal-Fetal Medicine. Electronic address: [email protected]; Hoskins IA, Combs CA. Society for Maternal-Fetal Medicine Special Statement: Updated checklists for management of monochorionic twin pregnancy. Am J Obstet Gynecol. 2020 Nov;223(5): B16-B20. doi: 10.1016/j.ajog.2020.08.066.
66.    Salomon LJ, Alfirevic Z, Berghella V, Bilardo C, Hernandez-Andrade E, Johnsen SL, Kalache K, Leung KY, Malinger G, Munoz H, Prefumo F, Toi A, Lee W; ISUOG Clinical Standards Committee. Practice guidelines for performance of the routine mid-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol. 2011 Jan;37(1):116-26. doi: 10.1002/uog.8831.
67.    Ong SSC, Zamora J, Khan KS, Kilby MD. Prognosis for the co-twin following single-twin death: a systematic review. BJOG 2006; 113: 992 – 998. doi: 10.1111/j.1471-0528.2006.01027. x.
68.    Hillman SC, Morris RK, Kilby MD. Co-twin prognosis after single fetal death: a systematic review and meta-analysis. Obstet Gynecol 2011; 118: 928 – 940. doi: 10.1097/AOG.0b013e31822f129d. 
69.    Shek NW, Hillman SC, Kilby MD. Single-twin demise: Pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 2014; 28: 249 – 263. doi: 10.1016/j.bpobgyn.2013.11.003. 
70.    Simonazzi G, Segata M, Ghi T, Sandri F, Ancora G, Bernardi B, Tani G, Rizzo N, Santini D, Bonasoni P, Pilu G. Accurate neurosonographic prediction of brain injury in the surviving fetus after the death of a monochorionic cotwin. Ultrasound Obstet Gynecol. 2006 May;27(5):517-21. doi: 10.1002/uog.2701. 
71.    van Klink JM, van Steenis A, Steggerda SJ, Genova L, Sueters M, Oepkes D, Lopriore E. Single fetal demise in monochorionic pregnancies: incidence and patterns of cerebral injury. Ultrasound Obstet Gynecol. 2015 Mar;45(3):294-300. doi: 10.1002/uog.14722.
72.    Booker W, Fox NS, Gupta S, Carroll R, Saltzman DH, Klauser CK, Rebarber A. Antenatal Surveillance in Twin Pregnancies Using the Biophysical Profile. J Ultrasound Med. 2015 Nov;34(11):2071-5. doi: 10.7863/ultra.14.12063.
73.    Burgess JL, Unal ER, Nietert PJ, Newman RB. Risk of late-preterm stillbirth and neonatal morbidity for monochorionic and dichorionic twins. Am J Obstet Gynecol 2014; 210: 578.e1 – 9. doi: 10.1016/j.ajog.2014.03.003.
74.    Russo FM, Pozzi E, Pelizzoni F, Todyrenchuk L, Bernasconi DP, Cozzolino S, et al. Stillbirths in singletons, dichorionic and monochorionic twins: a comparison of risks and causes. Eur J Obstet Gynecol Reprod Biol 2013; 170:131–6. doi: 10.1016/j.ejogrb.2013.06.014.
75.    Baxi LV, Walsh CA. Monoamniotic twins in contemporary practice: a single-center study of perinatal outcomes. J Matern Fetal Neonatal Med. 2010 Jun;23(6):506-10. doi: 10.3109/14767050903214590.
76.    DeFalco LM, Sciscione AC, Megerian G, Tolosa J, Macones G, O’Shea A et al. Inpatient versus outpatient management of monoamniotic twins and outcomes. Am J Perinatol 2006; 23:205 –11. doi: 10.1055/s-2006-934091.
77.    Ezra Y, Shveiky D, Ophir E, Nadjari M, Eisenberg VH, Samueloff A et al. Intensive management and early delivery reduce antenatal mortality in monoamniotic twin pregnancies. Acta Obstet Gynecol Scand 2005; 84:432–5. doi: 10.1111/j.0001-6349.2005.00683. x.

Please note that the maximum upload size is 5MB, and larger images and video clips can be sent to [email protected].