Anomalies of the placenta and umbilical cord in twin...

ajog.org Obstetrics Expert Reviews

Anomalies of the placenta and umbilical cord intwin gestationsCorinne Hubinont, MD, PhD; Liesbeth Lewi, MD, PhD; Pierre Bernard, MD; Etienne Marbaix, MD, PhD;Frederic Debieve, MD, PhD; Eric Jauniaux, MD, PhD

ith the development of new

The frequency of twin gestations has increased over the last few decades, mainlydue to maternal age at childbearing, and the use of assisted reproductive tech-nologies. Twins are at higher risk of aneuploidy, structural anomalies, and placentalabnormalities. Some of the placental and umbilical cord abnormalities found in twingestations are nonspecific and can be found in singleton gestations (ie, placentaprevia, placental abruption, single umbilical artery, velamentous cord insertion, vasaprevia, etc). However, other anomalies are unique to twin gestations, and aremainly associated with monochorionic twinsethese include intraplacental anasto-mosis and cord entanglement. Most of these conditions can be diagnosed withultrasound. An accurate and early diagnosis is important in the management oftwin gestations. Determination of chorionicity, amnionicity, and the identification ofplacental anomalies are key issues for the adequate management of twin preg-nancies. Pathologic placental examination after delivery can help in assessing thepresence of placental and umbilical cord abnormalities, as well as providing in-formation about chorionicity and gaining insight into the potential mechanisms ofdisease affecting twin gestations.

Key words: chorionicity, cord entanglement, discordant growth, fetal placental ratio,intertwin septum, multiple gestation, twin to twin transfusion syndrome, vascular ana-tomosis, zygosity

W assisted reproductive techniques(ART) in the late 1970s, multiple ges-tation pregnancy rates have increasedmarkedly around the world. In theUnited States, the rate of twin pregnan-cies has stabilized at 32 per 1000 birthsin 2006.1 The latest Centers for DiseaseControl and Prevention report on ARTsurveillance indicates that 43% of ART-conceived infants in 2011 in the UnitedStates were twins.2

Twinning is associated with higherincidence of perinatal risks for bothmothers and fetuses compared tosingleton pregnancies. The main risksare early and late miscarriage, pre-eclampsia, antepartum bleeding, post-partum hemorrhage, preterm delivery,intrauterine growth restriction (IUGR),and stillbirths.1-5 Twins are also moreprone to birth asphyxia, hyaline mem-brane disease, respiratory disorders, sei-zures, and long-term developmentalmorbidity.1-5 Prematurity and its com-plications is the single most importantcause of perinatal morbidity and

From the Departments of Obstetrics(Drs Hubinont, Bernard, and Debiève) andPathology (Dr Marbaix), Saint Luc UniversityHospital, Université de Louvain, Brussels,Belgium; Department of Obstetrics, UniversityHospitals, Department of Development andRegeneration, Katholieke Universiteit Leuven,Leuven, Belgium (Dr Lewi); and Institute forWomen’s Health, University College LondonMedical School, London, United Kingdom(Dr Jauniaux).

Received May 6, 2015; revised June 24, 2015;accepted June 25, 2015.

Drs Hubinont, Bernard, and Debiève aresupported by the charity Fetus for Life.

The authors report no conflict of interest.

Corresponding author: Corinne Hubinont,MD, PhD. [email protected]

0002-9378/$36.00ª 2015 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ajog.2015.06.054

mortality in multiple pregnancies.6

Overall, perinatal mortality rates are re-ported to be 4-fold higher for twins thanfor singletons.1,3,5 Most of these com-plications are directly or indirectlyassociated with placental or umbilicalcord disorders.5

Twin pregnancies are obviously athigher risks for birth defects thansingleton due to the development of2 fetuses instead of 1.1,5,8 Cohort studieshave suggested that in vitro fertilization(IVF) could be associated with higherincidence of birth defects.7,8 How-ever, the lack of information on the eti-ology of the infertility, chorionicity,maternal preexisting medical condi-tions, parental smoking status, and socialenvironments in most studies hampersthe interpretation of the correspondingdata.7 A recent large Australian cohortstudy showed that the increased riskof birth defects associated with IVF isno longer significant after adjustmentfor parental factors.8 However, placenta

OCTOBER 2015 Am

previa and velamentous cord insertion(VCI) are more common in singletonIVF than in spontaneous pregnanciessuggesting the incidence of placentaland cord anomalies can be influencedby the mode of conception.4,7

Development, position, and vascu-larity abnormalities of the placenta andthe umbilical cord can impact signifi-cantly perinatal morbidity and mortal-ity. The aim of this review is to providean outline of these anomalies associatedwith the twinning process and discussthe corresponding pathophysiologyand diagnostic features. Most of thesepathologies can be diagnosed in uteroby routine ultrasound examination andshould be an integral part of prenatalinvestigations in twins.4,5,9 For a betterunderstanding of the pathogenesis, itis essential to confirm the prenataldiagnosis with a detailed histopatho-logical placenta examination at birth.Placental and cord pathologies aretraditionally divided into primary or

erican Journal of Obstetrics & Gynecology S91

mailto:[email protected]

http://dx.doi.org/10.1016/j.ajog.2015.06.054

http://www.AJOG.org

FIGURE 1Ultrasound chorionicity diagnosis

Ultrasound of intertwin membranes at level of placental insertion in dichorionic-diamniotic twins with

fused placentas showing lambda sign (left) and in monochorionic-monoamniotic pregnancy showing

T sign (right).

Hubinont. Placental and cord disorders in twin gestations. Am J Obstet Gynecol 2015.

Expert Reviews Obstetrics ajog.org

congenital anomalies such as tumors andsecondary anomalies such as throm-bosis. For the purpose of our review,we have analyzed these anomalies ac-cording their specific and nonspecificassociation with twin pregnancies.

Zygosity vs chorionicityZygosity and chorionicity are distinctentities. A dichorionic (DC)-diamniotic(DA) placenta can be found in bothmonozygotic (MZ) and dizygotic twins

FIGURE 2Ultrasound of monochorionicmonaamniotic twin pregnancy

First-trimester ultrasound of monochorionic-

monoamniotic twin pregnancy showing single

sac and twisted umbilical cords or Y sign (arrow).

Hubinont. Placental and cord disorders in twin gestations.Am J Obstet Gynecol 2015.

S92 American Journal of Obstetrics & Gynecology

whereas a single ormonochorionic (MC)placenta mass is mainly associated withMZ twins.10 Zygosity or twins classifica-tion based on a double or a single fertil-ization cannot be predicted in DCsimilar gender twins.11 The low incidenceof MZ twinning is constant worldwideand seems independent of environmen-tal factors.1,2 However, ART and mainlyIVF increase both the incidence of MZbut also MC twins.3,4

Zygosity is generally establishedpostnatally using genetic tests on um-bilical cord blood. Quantitative fluo-rescent polymerase chain reactionamplification of microsatellite markershas been performed antenatally on fetal/placental cells obtained from amnio-centesis or chorionic villous samplingfor scientific purposes.12 Noninvasiveprenatal determination of twin zygosityusing maternal plasma free fetal DNAsequencing similar to that used for theaneuploidy testing has recently beenreported.13

Independently of the conceptionmode, the fetal, placental, and cord ano-malies risk depends mainly on the cho-rionicity and amnionicity in twins.1,4,5,14

Overall, perinatal mortality is around11% in MC twins compared to 5.0%in DC twins.1,5,14 Monoamniotic (MA)twins are rare (1% of MZ twins) butassociated with the highest morbidity

OCTOBER 2015

and mortality rate of all different typesof twinning.9,15,16 An early determina-tion of chorionicity and amnionicityis therefore essential to optimize themanagement pathways in twin pregnan-cies.17-20 The optimal window to deter-mine chorionicity in twins with 98%accuracy is at 7-9 weeks of gestation.18

Accuracy may be higher for DC twinsthan MC twins and is related to the ges-tational age at which the sonographicappearance of the amniotic sac develops.

Ultrasound examination of twin preg-nancies at 10-14 weeks of gestation pre-dicts chorionicity with a high degree ofaccuracy using a combination of thenumber of placentas, lambda and Tsigns,and intertwin membrane thickness.17-19

Two distinct placental masses and diff-erent fetal gender indicate DC. Whenonly 1 placental mass is visible on ultra-sound, the presence of a lambda signat the insertion of the intertwin mem-branes is an accurate predictor for DCwhereas T sign is the most reliable indi-cator of MC (Figure 1).17-20 Measure-ments of the intertwin membranethickness and membrane layer count areassociated with a lower sensitivity andspecificity than the ultrasound featuresused earlier in pregnancy but can beuseful to determine chorionicity duringthe second trimester of pregnancy whenthe insertion of the intertwin is lessclear.20

MA is determined by the absence ofa dividing membrane between the am-niotic sacs.11,15,17 MA should be sus-pected at 10-14 weeks in the presence ofa single amniotic sac and closely insertedumbilical cords (Figure 2). The numberof yolk sacs is not always an accuratesonographic sign of amnionicity.21,22

Twin-specific anomalies of theplacenta and umbilical cordPlacental vascular anastomosesNearly all MC placentas have vascularconnections or anastomoses between the2 umbilical-placental circulations.23-28

Postdelivery placental examination in-jections studies have shown that theyare located either superficially on thefetal surface or more deeply insidethe placental mass24-27 (Figure 3). Threedifferent types of anastomoses have

http://www.AJOG.org

FIGURE 3Placental circulation inuncomplicated twin pregnancy

Injection study of placental circulations in

uncomplicated monochorionic-diamniotic twin

pregnancy at 36 weeks of gestation.



been described: arterioarterial (AA),arteriovenous (AV), and venovenous(VV) (Figure 4).

Their role in twin’s morbidity is wellestablished since early studies havesuggested that in twin-twin trans-fusion syndrome (TTTS) there is animportant blood flow transfer throughunidirectional AV anastomoses withan insufficient compensatory counter-transfusion.25,26,28,29

AA anastomoses. These anastomoses aregenerally superficial and bidirection-al.24,27 Their frequency varies but theirpresence seems to be associated with aprotective effect for many of the com-plications of MC (Figure 4). A recentcase-control series has found that AAanastomoses are present in 37% of TTTSplacentas compared to 91% in controlnon-TTTS placentas (P < .001).28 AAanastomoses are also less frequent intwin anemia-polycythemia sequence(TAPS). TAPS is a particular form ofintertwin transfusion imbalance, whichis characterized by a difference in he-moglobin without the amniotic fluiddiscordance typical for chronic TTTS.30

When AA anastomoses are present inTAPS, they have a smaller diameter thanthose found in placentas from controltwin pregnancies (Figure 5).30,31

AA anastomoses can be demonstratedby color Doppler ultrasound imagingand are characterized by cyclic changesin systolic velocities with intermittentreversal of end-diastolic velocities.32,33 Acomputer model has shown that thistypical waveform pattern is the resultof 2 opposing pulsatile blood flowwaveforms with different velocities andfrequencies.32 In TTTS, the survival rateis better when AA anastomoses arepresent.33

AA anastomoses may also play a rolein the pathophysiology of the twinreversed arterial perfusion sequence,MCMA twinning, and morbidity afterintrauterine death of 1 twin.24 In thelatter, AA anastomoses are associatedwith a higher morbidity in the survivingcotwin.32 In twin fetuses presentingwith discordant growth with unequallyshared placentas, an increase in the AAanastomoses diameter is associated with

a reduced birthweight discordance. Thisis attributed to a rescue blood transferthrough AA anastomoses to the smallertwin.34

AV anastomoses. They are present in95% of MC placenta, are unidirectional,and are located in the depth of theplacenta.24,34When they are unbalanced,AV anastomoses are responsible for theoccurrence of the main complications ofMC including TTTS, TAPS, and severegrowth discordance (Figure 4).25-29 InTTTS, there is at least 1 unidirectionalAV anastomosis and a paucity of super-ficial anastomoses.25,29,33 Because oftheir location inside the placental mass,their exact number is difficult to evalu-ate even under direct fetoscopic vision.This can explain some of the therapeuticfailures observed with laser coagula-tion.24 Postfetoscopy iatrogenic TAPSmay result from small (<1 mm) intra-placental AVanastomosesmissed by lasercoagulation.24,31,35 TAPS may be associ-ated with a specific placental feature, adichotomy with the placental part of theanemic twin appearing hyperechogenicon ultrasound and hyperhemic atplacental examination (Figure 6).36

VV anastomoses. They are superficial,bidirectional, and present in only onequarter of MC placentas (Figure 4). Theclinical significance of VV anastomosesis still inconclusive and controversial.Their presence in MC placenta is asso-ciated with a 2-fold increase in the riskof TTTS compared to cases with noVV.24-27 A recent study has shown thatVV anastomoses are associated withTTTS and their presence is an indepen-dent risk factor for its development.37

Angioarchitecture patterns in MCMAtwins.MCMA placentas have a highernumber of AA, lower number of AV, anda similar number of VV anastomosesthan MCDA placentas.24,38,39 (Figure 7).This specific vascular pattern couldexplain the low incidence of TTTS inMCMA twins.39 Large-diameter AAanastomoses are generally present be-tween the 2 umbilical cord circulationsin MCMA placentas. This could explainpartly the high incidence of discordantcongenital anomalies found in MCMA

OCTOBER 2015 Am

twins. Brain and cardiac anomalies mayresult mainly from transfusion imbal-ances in the placental circulation duringembryogenesis but others defects may beassociated with early zygotic abnormalsplitting, fusion event, genetic or envi-ronmental factors.9,24,39

Discordant growth in twins andplacental functionTwin pregnancy is a specific conditionin which placental development isphysically constrained. Not surprisingly,IUGR is more frequent in twins com-pared to singletons.1,3,40-47 Poor growthaffecting both twins may reflect a generaluteroplacental dysfunction whereas adiscordant twin growth may be attrib-uted to several factors such as geneticgrowth potential differences betweencotwins, placental dysfunction confinedto 1 placenta, or unequal share of theplacental territory in MC placenta.40

Discordant growth between twinsis defined by a birthweight difference>25% between the 2 fetuses. It occurswith a similar incidence of 10-15%in both DC and MC twins.24,34 Select-ive IUGR (sIUGR) is defined by anestimated fetal weight <10th centileaffecting one of the twins. Recent studieshave suggested that first-trimestercrown-rump length evaluation could


http://www.AJOG.org

FIGURE 4Types, characteristics, physiopathological effects, and incidence ofvascular anastomoses in monochorionic placentas

AV, arteriovenous; IUFD, intrauterine fetal death; MC, monochorionic; TAPS, twin anemia polycythemia sequence; TRAP, twin reversedarterial perfusion sequence; TTTS, twin to twin transfusion syndrome.



predict the outcome in twin pregnanciesbut this is controversial.45,46

The gestational age at diagnosis of thegrowth discordance is also importantfor the prognosis. An early IUGR (diag-nosed <20 weeks) is associated witheither unequal placental sharing orearly transfusion unbalances in MCtwins and with placental pathologiesin DC twins.42,43,47 Twins with anearly-onset discordant growth have anoverall lower survival rate than those


with late-onset discordant and thosewith concordant growth (83% vs 96%vs 99%; P < .001).43,47

Discordant fetal growth in MC twins. InMC twins, IUGR is generally due tounequal placental sharing with ahigh blood flow transfusion from onetwin to the other through large-diameterAV anastomoses.23,24,34,41,42 A rescueconnecting vessel can protect thesmaller twin. If the intertwin transfusion

OCTOBER 2015

volume is high in this rescue vessel, therisk of major growth discordance islow.24,39-43 In case of early-onset dis-cordant growth, the placentas are moreunequally shared, having more andlarger AA anastomoses compared withplacentas with late-onset discordant orconcordant growth.43

The severity of sIUGR can be evalu-ated according to placental characteris-tics and blood flow in the umbilicalarteries. Type I presents with unequallyshared placental mass, average size AAanastomoses, and normal umbilicalartery Doppler measurements. Type IIis characterized by unequally sharedplacenta, absent or small AA anastomo-ses, and continuous increased resis-tance to blood flow in the umbilicalartery (absent or reverse end-diastolicflow). Type III presents with major un-equal placental sharing, at least 1 largeAA anastomose, and an intermittentincreased resistance to blood flow in theumbilical artery.40-43

It has recently been found that MCtwin pregnancies complicated by TTTSand sIUGR are characterized by adecreased angiogenic activity reflectingan abnormal placentation process.44

Discordant fetal growth in DC twins. Themechanisms for IUGR in most DCtwins are not clearly known. Since twinfetuses share the same maternal envi-ronment during gestation, birthweightdiscordance is related to factors affect-ing growth of each individual fetus.Several hypotheses have been proposedsuch as genetic factors and physical in-teractions at implantation resulting ina less favorable placental insertion inthe uterus.40 Spiral artery physiologicalconversion may be restricted in theseareas, leading to an impaired vascularperfusion of the placenta later in preg-nancy. In one case report of discordantDC twins, the morphological study ofthe placental-decidual interface showedthe development of a rare condition,maternal floor infarcts in the smallertwin placenta responsible for uteropla-cental vascular insufficiency.48

In most twin studies, there is a cor-relation between placental and fetalweight. It has been suggested that the

http://www.AJOG.org

FIGURE 5Placenta with twinanemiapolycythemia sequence

Injection study of monochorionic-diamniotic

placenta with spontaneous twin anemia-

polycythemia sequence. Note small-diameter

arterioarterial anastomose (arrow) at 35 weeks.Reproduced, with permission, from Lewi et al.24


FIGURE 6Placental dichotomy

Placental dichotomy associated with spontaneous twin anemia-polycythemia sequence. Ultrasound

hyperechogenicity of donor twin placenta (left) and corresponding placental tissue hyperhemia

(right ).



placenta size is more responsible forgrowth restriction in twins than a pla-centation deficiency.49 As the resultsare not correlated with the growthdiscordance severity, the data interpre-tation is limited. Others factors couldbe involved for explaining growth dis-turbances in twins. Incomplete conver-sion of the uteroplacental circulationis associated with chronic ischemiareperfusion of the placental tissue andleads to intermittent perfusion of theintervillous space.49,50 The resulting ox-ygen fluctuation is a potent inducer ofoxidative stress and apoptosis in theplacenta.51,52 Trophoblastic apoptosisis increased in case of preeclampsiaand miscarriages and is linked directlywith oxidative stress.50,51 An excess ofplacental apoptosis and changes in syn-thesis of various trophoblastic proteinsare found in discordant DC twins con-firming the role of oxygenation, apo-ptosis, and oxidative stress in theirgrowth disturbance.53-54

Umbilical cord entanglementThis complication is specific of MCMAtwinning but has also been describedafter spontaneous and iatrogenous sep-tostomy in both MCDA and DCDAtwins.55-58 Cord entanglement can bedetected with ultrasound from 10 ges-tational weeks using the so-called “Ysign” (Figure 2). Cord entanglement hasbeen associated with a high incidenceof intrauterine fetal death.5,14,16,59 Aregular ultrasound follow-up using 2-dimensional or if available, 3-dimensionaland directional color Doppler imagingis recommended (Figure 8).17,60 How-ever, a recent systematic review has re-ported an overall survival rate as highas 88.6% suggesting that ultrasoundprenatal diagnosis of cord entanglementdid not improve neonatal outcome.59 Asmall cases series has also shown that thepresence of a notch in umbilical arterywaveform is not associated with anadverse perinatal outcome.61 Further-more, even in cases complicated withsevere TTTS requiring laser surgery,survival rate remains at 75%,62 con-firming a better perinatal outcome forMCMA pregnancies than previouslyreported.

Umbilical proximate cord insertionUmbilical cord development is essentialfor an ultimate fetal nutrition. A retro-spective study based on 11,980 twins’umbilical cords suggests a combinedinfluence of genetic and environmentalfactors on their morphological charac-teristics.63 One of them is the distancebetween the insertion of the cords inMCtwins placenta ranging from 4-25 cm atdelivery at term.64 A measurement<5thcentile (3.3-4 cm) is found in 5% of MCtwin pregnancies (Figure 7). It occursmore frequently in MCMA (53%) thanin MCDA (3%) placenta. The presenceof proximate cord insertion (PCI) inMC placenta is associated with a higherprevalence of AA and VVanastomoses.64

A reduced space between the 2 cordinsertions is probably not pathogenicbut the increased number of VV anas-tomoses associated with PCI is a well-established factor for adverse fetaloutcomes.37 In severe TTTS, the pres-ence of PCI has been associated withhigher rates of laser therapy failuresdue to technical difficulties in accessingthe placental equator and preventingall anastomoses from being coagulated

OCTOBER 2015 Am

during the procedure.64 The data onPCI have been exclusively obtained frommorphological placental examinationafter delivery and there are no data onprenatal sonographic prognostic evalu-ation of PCI in themanagement of twins.


http://www.AJOG.org

FIGURE 7Proximate umbilical cordinsertion

Injection study of monochorionic-monoamniotic

placenta with proximate umbilical cord insertion

and arterioarterial, venovenous, and arterio-

arterial anastomoses.



Intertwin septum anomaliesA disparity in fluid volume distributionbetween amniotic sacs creates a fold inthe intertwin membranes described as

FIGURE 8Cord entanglement

Ultrasound imaging of cord entanglement (a

A, Two-dimensional ultrasound at 32 weeks. B,

C, Three-dimensional color Doppler inversion modeHubinont. Placental and cord disorders in twin gestations. Am


the “folding sign.”65 It is generally asso-ciated with a discrepancy in the echo-genicity of amniotic fluid. In MCDAtwins, the absence of membrane foldingat 15-17 weeks is associated with a lowincidence (<2%) of TTTS compared tothe group with the folding sign subse-quently developing TTTS in 43%. Thisearly second-trimester ultrasound signis a good predictor of twins’ outcome.65

Surgical septostomy or accidentalrupture of the intertwin membraneduring fetoscopic laser photocoagula-tion for TTTS can increase the risksof complications such as cord entangle-ment.56,66-69 Septostomy can be associ-ated with amniotic membrane flapsand induce a pseudoamniotic bandsyndrome in 2-3% of the cases involvingthe limbs or the umbilical cord andleading to amputation and intrauterinedeath.70 Therapeutic septostomy iscontroversial in TTTS but has beenassociated with an improvement of fetaland neonatal morbidity, also due toconcomitant amniodrainage.57,71

rrow) in monochorionic-monoamniotic twins.

Directional color power Doppler at 28 weeks.

. D, Cord entanglement and twisting at delivery.J Obstet Gynecol 2015.

OCTOBER 2015

An intertwin membrane hematomais a rare complication of DCDA twinsgenerally associated with the develop-ment of a subchorionic hematoma un-der the insertion of the membrane. Onultrasound, it appears as a hypoecho-genicmass located between the intertwinmembranes and should be managed asmarginal placental abruption.72

Nonspecific placental and cordanomalies in twinsComplete hydatiform mole in twingestationA classic or complete hydatidiform mole(CHM) may coexist with a normal fetusand placenta in cases of molar trans-formation of 1 ovum in a dizygotic twinpregnancy.73,74 This rare complicationof twin gestation can be misdiagnosedduring the first trimester if the molartissue partially covers the normal pla-centa. An accurate detection of theCHM is possible at the end of the firsttrimester (Figure 9). The differentialdiagnosis includes mainly large cysticplacenta, mesenchymal dysplasia ofthe placenta, and degenerating uterinefibroids. As pregnancy advances, themarked generalized swelling of themolar tissue with large hemorrhagicareas can be more easily identified andmanaged accordingly. Twin pregnanciesincluding a CHM are at high risk ofdeveloping severe medical complicationssuch as preeclampsia, IUGR, and poorperinatal outcome.74

Placental lesionsSystematic reviews have confirmed theessential role of placental pathology,mainly inflammatory and vascular le-sions on the neonatal morbidity andmortality in singletons.75,76 In twins,these lesions are more frequent as theincidence of complications such as pre-term labor, premature rupture of themembranes, preeclampsia, and growthrestriction is increased.1,5,6 In case ofchorioamnionitis, nonspecific placentalanomalies such as funisitis, acute andchronic villitis, and deciduitis may befound postnatally.77 Placental vascularlesions prevalence is higher in twinsthan in singletons. Moreover, in MCplacenta, histopathology examination

http://www.AJOG.org

FIGURE 10Velamentous cord insertion

Velamentous cord insertion and vasa previa in

monochorionic-diamniotic placenta.


FIGURE 9Complete hydatiform mole coexisting with fetus

Ultrasound imaging of complete hydatiform mole (left ; arrow) coexisting with normal fetus at

11 weeks and macroscopic placental examination showing molar tissue at birth (right; arrow ).



shows a higher incidence of infarct-ions, subchorial fibrin deposition, andabnormal villous maturation com-pared to DC twins (41.5% vs 32.9%;P ¼ .009).78,79 MC twins present alsowith a higher incidence of fetal vesselsthrombosis compared to DC.80 Fetalvascular thrombosis is found generallyin association with IUGR in MC twinsand with hypertensive disorders in DCtwins.80 The increased incidence of pla-cental infarctions and thrombosis in DCtwin placentas compared to MC andsingletons may be associated with thehigher prevalence of preeclampsia in DCtwin pregnancies.81 These lesions aremore likely to be the consequences ofabnormal placentation rather than thecause of preeclampsia.

Placenta previaThe overall incidence of placenta previain twins has been reported to be 40%higher than in singletons after exclusionof confounding factors such as multi-gravida, advanced gestational age, andsmoking.82 However, a recent retro-spective study has found a similar inci-dence of placenta previa during thesecond trimester in singleton and twinpregnancies. In the vast majority of casesin both groups, the low placental loca-tion resolved spontaneously during thethird trimester.82 This controversialstudy may be explained by the lack ofknowledge about chorionicity.

Chorionicity is pivotal in evaluatingthe risk of placenta previa in twins andan increased risk has been found in DCtwins compared with singletons andMC twins.82,83 This is probably theconsequence of the presence of 2 devel-oping placental masses in DC twins. IVFtwins presents with an increased inci-dence of placenta previa than singletonand spontaneous twins.4,83 Determina-tion of placental location is part ofroutine prenatal ultrasound examina-tion and its diagnostic modality istransvaginal ultrasonography.

Morbidly adherent placentaThe incidence of placenta accreta (PA)hasincreased 10-fold since the early 1900sand directly correlates with the increasingcesarean delivery rate in most Western

countries.84 There are limited clinical dataon the diagnosis and management of PAin twin pregnancies. Three cases of deepPA (percreta) have been reported, allcomplicated by uterine rupture duringthe second trimester and requiring anemergency hysterectomy.85-87 Prenataldiagnosis by imaging followed by anadequate management by a multidisci-plinary team reduces significantly bothmorbidity and mortality associated withPA. The specific ultrasound featuresincluding the presence of placental la-cuna, absence of hypoechogenic line be-tween placenta and myometrium, andtransmyometrial bulging of placental si-nus at the myometrium and bladderinterface should bedetectedwith the sameaccuracy in twins.84

Placental abruptionThe risk of developing placental abrup-tion is 2-fold higher in twins com-pared to singletons.88,89 This can beexplained by the presence of 2 placentasbut also by cofactors such as maternalage, multiparity, premature rupture ofthe membranes, maternal anemia, andhypertensive-related disorders, whichare all increased in twin pregnancies.88-90

More recently, maternal weight hasbeen identify as an additional risk factorfor placental abruption with a prepreg-nancy body mass index<18.5 associatedwith a higher risk of placental abruptionin twin pregnancy compared to normaland obese women.91 Twin pregnanciescomplicated by vaginal bleeding in early

OCTOBER 2015 Am

pregnancy have an increased risk ofabruption.92 Finally there is also a theo-retical higher risk of abruption of oneof the placenta during delivery in thedelivery interval between the first andsecond twin. The development of a he-matoma between the placenta and theuterine wall is rarely observed on ultra-sound in the second half of pregnancyand the prenatal diagnosis is thereforebased on clinical symptoms.

Velamentous cord insertionand vasa previaAVCI of one of the umbilical cords is 8times more common in twins than insingletons. MC doubles the risk for VCI


http://www.AJOG.org

TABLERecommended morphologic examination of placenta in twins1. Identification and labeling of cords and placenta(s)2. Examination of membranes (layers, vasa previa)3. Number of placenta(s)4. Macroscopic examination of maternal and fetal placental sides5. Insertion of umbilical cords (velamentous, proximity)6. Number of vessels in cords (single umbilical artery)7. Placental weight and fetal to placental weight ratio8. In monochorionic twins, identification of vascular anastomoses with or without injection



and is associated with a contralateraldevelopment of the superficial angio-vasculature suggesting that early angio-genesis is dependent of umbilical cordinsertion in relation to the developmentof the definitive placenta.93-96 The inci-dence of VCI, vasa previa, or marginalcord insertion is higher in ART than inspontaneously conceived singletons butsimilar in both types of twins.4,7,97 Thereis a 3-fold increase in the incidence ofVCI in twins presenting with IUGRcompared to normally grown twins.96

In MC placenta, VCI is associated witha decreased blood flow in the umbil-icoplacental circulation with additionalrisk factor for the vascular thrombosisand development of TTTS.93-95

FIGURE 11Fetal:placental weight ratio as a funcand twin gestations

Evolution of fetal to placental weight ratio durin

dichorionic twin pregnancies.Adapted from Almog et al.110

Hubinont. Placental and cord disorders in twin gestations. Am


Vasa previa is a rare anomaly in bothsingleton and twin pregnancies but ismore common in twins due to the higherincidence of VCI, bilobated placenta,and placenta previa.98,99 (Figure 10).Vasa previa in twins has been associatedwith a higher but unexplained risk ofemergency preterm delivery comparedto singletons.99

Single umbilical arteryIn twins, the incidence of single umbilicalartery (SUA) is 3 times greater than insingletons (3% vs 1%) but similar in MCand DC twins.100-102 The fact that MCtwins can be discordant for SUA in MCtwins indicates that environmental factorsplay a role for determining the occurrence

tion of gestational age in singleton

g gestation in singleton, monochorionic, and

J Obstet Gynecol 2015.

OCTOBER 2015

of this anomaly.9,101 SUA twins are athigher risks of IUGRandpretermdelivery<28weeks.Twinpairs discordant for SUApresent with higher growth discordancethan those with normal umbilicalcords.100-103 The sonographic cross-sectional area of the SUA does notappear to show the typical adaptive dila-tation usually seen in singleton pregnan-cies with SUA.101 This apparent failure ofumbilical artery compensatory dilatationin twinswith SUAcould explain partly theincreased risk for IUGR in these cases.The prenatal diagnosis of SUA is pivotalfor the management of twins presentingwith discordant growth.

Postpartum placental examinationThe utility of histopathological exami-nation of the placenta and umbilicalcord after delivery is directly relevant tomany different aspects of perinatologyfrom the epidemiology of specific ob-stetric complications76,104 to malpracticelitigation.105

Morphological examination shouldstart in the delivery room with labellingof placentas and umbilical cords, usingdifferent size or shapes of clips (Table). Acomplete macroscopic report shouldinclude placental weight and membran-es examination, structure of intertwinmembranes, site of insertion and num-ber of vessels in each umbilical cord, andevaluation of vascular anastomoses inMC twins. In DCDA twins, there will be2 distinct or 1 fused mass of 2 placentasand 2 amniotic sacs separated by athick membrane. In MCDA twins,there will be a single placental massand the intertwin membrane appearstranslucent. In MCMA twins, no inter-twin membrane will be seen. A detaileddescription of the histopathology ofthe placenta in twins is available fromspecialized textbooks.10,23,106

Placental and umbilical cord-specificcharacteristics are found with an in-creased incidence in twin birthweightdiscordance.107 The evaluation of pla-centa to birthweight ratio or fetal toplacental weight ratio (FPR) also pro-vides indirect information on placentaldevelopment and function duringpregnancy. In singleton and twin preg-nancies, an abnormal FPR is a good

http://www.AJOG.org

FIGURE 12Milk injection of superficialplacental anastomoses

Demonstration of superficial placental anasto-

moses using milk injection in 1 cord vessel in

monochorionic-diamniotic placenta.



predictor for short- and long-termadverse outcome during childhood andadulthood such as cardiovascular dis-eases.108,109 Normogram and percentilecurves for placental weight and FPRhave been established for twin preg-nancies.110 An increased FPR reflects asmall placental size associated withplacental insufficiency.111 In twin gesta-tion, both birthweight and the FPR areincreased compared to singletons.110,112

The FPR increases throughout gesta-tion in singletons but remains stable intwins (Figure 11). During the thirdtrimester, FPR is higher in MC than inDC twins suggesting a higher degree ofplacental insufficiency in MC.112

Anomalies of the cord insertion are notcorrelated with FPR in MC or DC twins.The clinical implications of FPR changesin twin pregnancies remain to be evalu-ated but could be a predictor associationfor cardiovascular disease later in life.112

Gross placental lesions such as infarc-tion, thrombosis, and fibrin deposition,and cord with SUA are often found intwin pregnancies complicated by IUGRand/or growth discordance.78,79,107

In MC twins complicated by TTTS,anastomoses can only be accuratelyevaluated by injection studies (Figures 3,5, and 7) but these techniques requirespecific equipment and expertise.24,106 Asimplified method using milk injectionin cord vessels after clamping can behelpful to identify superficial vascularanastomoses (Figure 12).

ConclusionsPerinatal data suggest that in humanbeings, the high rate of complicationsobserved in twin pregnancies is linkedto specific pathophysiological changesin the placentation process. MC twinshave higher rates of perinatal mortality,growth discrepancies, and IUGR of bothfetuses than DC twins. This suggests thatthese complications could be related tospecific placental angioarchitecture ofMC twinning. In MC twins, the mostfrequent causes for growth restrictionare intertwin transfusion unbalances andunequal placental sharing. In DC twins,second- and third-trimester IUGR isgenerally associated with either primaryabnormal cord location or uteropla-cental vascular insufficiency.Most placental and cord anomalies

can be diagnosed accurately using ul-trasound before delivery. Prenatal diag-nosis of anomalies such as placentalanastomoses, SUA, or vasa previa have adirect impact on the obstetrical man-agement. Placental morphological ex-amination in twins can provide essentialinformation for evaluating perinataloutcome epidemiology. It can contri-bute toward a better understanding ofintrauterine environment in twin preg-nancies. Future research correlatingantenatal findings and postnatal histo-pathological assessment from multiplestudies into larger data sets will allowdelineation of distinctive clinicopatho-logical associations and further under-standing of pathophysiology of complexplacenta and cord anomalies in twins.-

REFERENCES

1. Chauhan S, Scardo J, Hayes E,Abuhamad A, Berghella V. Twins: prevalence,problems, and preterm births. Am J ObstetGynecol 2010;203:305-15.

OCTOBER 2015 Am

2. Sunderam S, Kissin DM, Crawford SB,Folger SG, Jamieson DJ, Barfield WD; Centersfor Disease Control and Prevention (CDC).Assisted reproductive technology surveillanceeUnited States, 2011. MMWR Surveill Summ2014;63:1-28.3. The ESHRE Capri Workshop Group. Multiplegestation pregnancy. Hum Reprod 2000;15:1856-64.4. Jauniaux E, Ben-Ami I, Maymon R. Doassisted-reproduction twin pregnancies requireadditional antenatal care? Reprod BiomedOnline 2013;26:107-19.5. Steenhaut P, Hubinont C. Perinatal mortalityin multiple pregnancy. In: Ezechi OC,Pettersson KO, eds. Perinatal mortality. Croatia:In Tech Europe; 2015. Available at: www.intechopen.com. Accessed July 28, 2015.6. Conde Agudelo A, Romero R. Predictionof preterm birth in twin gestations using bio-physical and biochemical tests. Am J ObstetGynecol 2014;211:583-95.7. Jauniaux ERM. Multiple gestation pregnancyafter assisted reproductive technology. In:Jauniaux ERM, Risk RMB, eds. Pregnancy af-ter assisted reproductive technology. Cam-bridge: Cambridge University Press; 2012:82-92.8. Davies MJ, Moore VM, Willson KJ, et al.Reproductive technologies and the risk of birthdefects. N Engl J Med 2012;366:1803-13.9. McNamara HC, Kane SC, Craig JM, ShortRV, Umstad MP. A review of the mechanismsand evidence for typical and atypical twinning.Am J Obstet Gynecol (in press).10. Krauss FT, Redline RW, Gersell DJ, NelsonDM, Dicke JM. Multiple pregnancy. In: Placentalpathology. Atlas of nontumor pathology, Edt.American Registry of Pathology, Washington,DC: 2004:249-82.11. Scardo JA, Ellings JM, Newman RB. Pro-spective determination of chorionicity, amniocityand zygosity in twin gestations. Am J ObstetGynecol 1995;173:1376-80.12. Cirigliano V, Canadas P, Plaja A, et al.Rapid prenatal diagnosis of aneuploidies andzygosity in multiple pregnancies by amniocen-tesis with single insertion of the needle andquantitative fluorescent PCR. Prenat Diagn2003;23:629-33.13. Qu JZ, Leung TY, Liao GJ, et al. Non inva-sive prenatal diagnosis of twin zygosity bymaternal plasma DNA analysis. Clin Chem2013;59:427-35.14. Kristiansen M, Joensen B, Ekelund C,Petersen O, Sandager P; with the Danish FetalMedicine Study Group. Perinatal outcome afterfirst-trimester risk assessment in monochorionicand dichorionic twin pregnancies: a population-based register study. BJOG 2015 http://dx.doi.org/10.1111/1471-0528.13326 [Epub ahead ofprint].15. Constantine S, Wilkinson C. Double trouble:the importance of reporting chorionicity andamnionicity in twin pregnancy ultrasound re-ports. J Med Imaging Radiat Oncol 2015;59:66-9.


http://refhub.elsevier.com/S0002-9378(15)00667-5/sref1

















http://www.intechopen.com

http://www.intechopen.com




























http://dx.doi.org/10.1111/1471-0528.13326

http://dx.doi.org/10.1111/1471-0528.13326






http://www.AJOG.org


16. Van Mieghem T, De Heus R, Lewi L, et al.Prenatal management of monoamniotic twinpregnancies.ObstetGynecol 2014;124:498-506.17. Hubinont C, Santolaya-Forgas J. A sys-tematic approach to first-trimester ultrasoundassessment of twins. Am J Perinatol 2010;27:595-8.18. Bora SA, Papageorghiou AT, Bottomley C,Kirk E, Bourne T. Reliability of transvaginalultrasonography at 7-9 weeks’ gestation in thedetermination of chorionicity and amnionicityin twin pregnancies. Ultrasound Obstet Gynecol2008;32:618-21.19. Carroll SG, Soothill PW, Abdel-Fattah SA,Porter H, Montague I, Kyle PM. Prediction ofchorionicity in twin pregnancies at 10-14 weeksof gestation. BJOG 2002;109:182-6.20. Blumenfeld YJ, Momirova V, Rouse DJ,et al. Eunice Kennedy Shriver National Instituteof Child Health and Human DevelopmentMaternaleFetal Medicine Units Network. Accu-racy of sonographic chorionicity classificationin twin gestations. J Ultrasound Med 2014;33:2187-92.21. Shen O, Samueloff A, Beller U,Rabinowitz R. Number of yolk sacs does notpredict amniocity in early first-trimester mono-chorionic multiple gestations. UltrasoundObstetGynecol 2006;27:53-6.22. Murakoshi T, Ishii K, Matsushita M,Shinno T, Naruse H, Torii Y. Monochorionicmonoamniotic twin pregnancies with two yolksacs may not be a rare finding: a report of twocases. Ultrasound Obstet Gynecol 2010;36:384-6.23. Benirschke K, Burton GJ, Baergen RN.Multiples pregnancies. In: Pathology of thehuman placenta, 6th ed. Berlin, Germany:Springer-Verlag Berlin Heidelberg; 2012.24. Lewi L, Deprest J, Hecher K. The vascularanastomoses in monochorionic twin pregnan-cies and their clinical consequences. Am JObstet Gynecol 2013;208:19-30.25. Bajoria R, Wigglesworth J, Fisk NM.Angioarchitecture of monochorionic placentasin relation to the twin-twin transfusion syndrome.Am J Obstet Gynecol 1995;172:856-63.26. Bermúdez C, Becerra CH, Bornick PW,AllenMH, Arroyo J, Quintero RA. Placental typesand twin-twin transfusion syndrome. Am JObstet Gynecol 2002;187:489-94.27. De Paepe ME. Examination of the twinplacenta. Semin Perinatol 2015;39:27-35.28. de Villiers SF, Slaghekke F, Middeldorp JM,Walther FJ, Oepkes D, Lopriore E. Arterio-arterial vascular anastomoses in monochorionicplacentas with and without twin-twin transfusionsyndrome. Placenta 2012;33:652-4.29. Fisk NM, Duncombe GJ, Sullivan MH. Thebasic and clinical science of twin-twin trans-fusion syndrome. Placenta 2009;30:379-90.30. de Villiers S, Slaghekke F, Middeldorp JM,et al. Arterio-arterial vascular anastomoses inmonochorionic twin placentas with and withouttwin anemia-polycythemia sequence. Placenta2012;33:227-9.

S100 American Journal of Obstetrics & Gynecolog

31. Van Meir H, Slaghekke F, Lopriore E, VanWijngaarden WJ. Arterio-arterial anastomosesdo not prevent the development of twin anemia-polycythemia sequence. Placenta 2010;31:163-5.32. Hecher K, Jauniaux E, Campbell S,Deane C, Nicolaides K. Artery-to-artery anas-tomosis in monochorionic twins. Am J ObstetGynecol 1994;171:570-2.33. Denbow ML, Cox P, Talbert D, Fisk NM.Color Doppler energy insonation of placentalvasculature in monochorionic twins: absentarterio-arterial anastomoses in association withtwin-to-twin transfusion syndrome. Br J ObstetGynaecol 1998;105:760-5.34. Lewi L, CannieM, Blickstein I, et al. Placentalsharing, birthweight discordance and vascularanastomoses in monochorionic diamniotic twinplacentas. Am J Obstet Gynecol 2007;197:587.e1-8.35. Van Winden KR, Quintero RA,Kontopoulos EV, et al. Preoperative twin anemiapolycythemia in the setting of twin twin trans-fusion syndrome (TTTS). Fetal Diagn Ther2015;37:274-80.36. Stritze A, Thomas S, Somerset D. Placentaldichotomy: a hint in twin anemia polycythemiasequence. J Obstet Gynaecol Can 2014;36:1097-100.37. De Villiers SF, Zhao DP, Cohen D, et al.Correlation between veno-venous anastomo-ses, TTS and perinatal mortality in mono-chorionic twin pregnancies. Placenta 2015;36:603-6.38. Bajoria R. Abundant vascular anastomosesin monoamniotic versus diamniotic mono-chorionic placentas. Am J Obstet Gynecol1998;179:788-93.39. Umur A, van Gemert MJ, Nikkels PG.Monoamniotic-versus diamniotic-monochorionictwin placentas: anastomoses and twin-twintransfusion syndrome. Am J Obstet Gynecol2003;189:1325-9.40. Lewi L, Devlieger R, De Catte L, Deprest J.Growth discordance. Best Pract ResClin ObstetGynaecol 2014;28:295-303.41. Valsky DV, Eixarch E, Martinez JM, Crispi F,Gratacós E. Selective intrauterine growth re-striction in monochorionic twins: pathophysi-ology, diagnostic approach and managementdilemmas. Semin Fetal Neonatal Med 2010;15:342-8.42. Gratacós E, Ortiz JU, Martinez JM.A systematic approach to the differential diag-nosis and management of the complicationsof monochorionic twin pregnancies. Fetal DiagnTher 2012;32:145-55.43. Lewi L, Gucciardo L, Huber A, et al. Clinicaloutcome and placental characteristics of mon-ochorionic diamniotic twin pairs with early- andlate-onset discordant growth. Am J ObstetGynecol 2008;199:511.e1-7.44. Yinon Y, Ben Meir E, Berezowsky A, et al.Circulating angiogenic factors in monochorionictwin pregnancies complicated by twin-to-twintransfusion syndrome and selective intrauterine

y OCTOBER 2015

growth restriction. Am J Obstet Gynecol2014;210:141.e1-7.45. Johansen ML, Oldenburg A, Rosthøj S,Cohn Maxild J, Rode L, Tabor A. Crown-rumplength discordance in the first trimester: apredictor of adverse outcome in twin preg-nancies? Ultrasound Obstet Gynecol 2014;43:277-83.46. D’Antonio F, Khalil A, Dias T,Thilaganathan B; Southwest Thames ObstetricResearch Collaborative. Crown-rump lengthdiscordance and adverse perinatal outcome intwins: analysis of the Southwest Thames Ob-stetric Research Collaborative (STORK) multiplepregnancy cohort. Ultrasound Obstet Gynecol2013;41:621-6.47. D’Antonio F, Khalil A, Thilaganathan B;Southwest Thames Obstetric Research Collab-orative (STORK). Second-trimester discordanceand adverse perinatal outcome in twins: theSTORK multiple pregnancy cohort. Br J ObstetGynecol 2014;121:422-9.48. Redline RW, Jiang JG, ShahD. Discordancyfor maternal floor infarction in dizygotic twinplacentas. Hum Pathol 2003;34:822-4.49. Bleker OP,Wolh H, Oosting J. The placentalcause of fetal growth retardation in twin gesta-tion. Acta Genet Med Gemellol (Roma) 1995;44:103-6.50. Khong TY, De Wolf F, Robertson WB,Brosens I. Inadequate maternal vascularresponse to placentation in pregnancies com-plicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol1986;93:1049-59.51. Burton GJ, Jauniaux E. Oxidative stress.Best Pract Res Clin Obstet Gynaecol 2011;25:287-99.52. Burton GJ, Jauniaux E, Charnock-Jones DS. The influence of the intrauterineenvironment on human placental development.Int J Dev Biol 2010;54:303-12.53. Almog B, Shehata F, Aljabri S, et al.Placental apoptosis in discordant twins. Pla-centa 2002;23:331-6.54. Matsubara S, Minakami H, Sato I. Placentaof discordant twins: lack of change in histo-chemically detectable enzyme activities. TwinRes 2000;3:123-8.55. Jeanty C, Newman E, Jeanty P, Rodts-Palenik S. Prenatal diagnosis of spontaneousseptostomy in dichorionic diamniotic twinsand review of the literature. J Ultrasound Med2010;29:455-63.56. Bevilacqua E, Aliberti C, D’Ambrosio V,Giancotti A, Perrone G, La Torre R. Sponta-neous septostomy in monochorionic diamniotictwins: difficult diagnosis, difficult management.J Obstet Gynaecol 2014;34:359.57. Hubinont C, Bernard P, Magritte JP,Donnez J. Nd:YAG laser and needle disruptionof the interfetal septum: a possible therapy insevere twin-to-twin transfusion syndrome.J Gynecol Surg 1996;12:183-9.58. Arabin B, Laurini RN, van Eyck J. Earlyprenatal diagnosis of cord entanglement in







































































































































































































http://www.AJOG.org


monoamniotic multiple pregnancies. UltrasoundObstet Gynecol 1999;13:181-6.59. Kuwata T, Matsubara S, Suzuki M. 3D ColorDoppler of monoamniotic twin cord entangle-ment. Arch Gynecol Obstet 2010;281:973-4.60. Rossi AC, Prefumo F. Impact of cord entan-glement on perinatal outcome of monoamniotictwins: a systematic review of the literature. Ultra-sound Obstet Gynecol 2013;41:131-5.61. Aurioles-Garibay A, Hernandez-Andrade E,Romero R, et al. Presence of an umbilical arterynotch in monochorionic/monoamniotic twins.Fetal Diagn Ther 2014;36:305-11.62. Peeters SH, Devlieger R, Middeldorp JM,et al. Fetal surgery in complicated mono-amniotic pregnancies: case series and sys-tematic review of the literature. Prenat Diagn2014;34:586-91.63. Antoniou EE, Derom C, Thiery E, Fowler T,Southwood TR, Zeegers MP. The influenceof genetic and environmental factors on the eti-ology of the human umbilical cord: the EastFlanders prospective twin survey. Biol Reprod2011;85:137-43.64. Zhao DP, Peeters SH, Middeldorp JM,et al. Monochorionic placentas with proximateumbilical cord insertions: definition, prevalenceand angio-architecture. Placenta 2015;36:221-5.65. Sebire NJ, Souka A, Skentou H, Geerts L,Nicolaides KH. Early prediction of severe twin-to-twin transfusion syndrome. Hum Reprod2000;15:2008-10.66. Feldman DM, Odibo A, Campbell WA,Rodis JF. Iatrogenic monoamniotic twins asa complication of therapeutic amniocentesis.Obstet Gynecol 1998;91:815-6.67. Cook TL, O’Shaughnessy R. Iatrogeniccreation of a monoamniotic twin gestation insevere twin-twin transfusion syndrome. J Ultra-sound Med 1997;16:853-5.68. Cruz-Martinez R, Van Mieghem T, Lewi L,et al. Incidence and clinical implications of earlyinadvertent septostomy after laser therapy fortwin-twin transfusion syndrome. UltrasoundObstet Gynecol 2011;37:458-62.69. Peeters SH, Stolk TT, Slaghekke F, et al.Iatrogenic perforation of intertwin membraneafter laser surgery for twin-to-twin transfusionsyndrome. UltrasoundObstet Gynecol 2014;44:550-6.70. Ting YH, Lao TT, Law KM, Cheng YK,Lau TK, Leung TY. Pseudoamniotic band syn-drome after in utero intervention for twin-to-twintransfusion syndrome: case reports and litera-ture review. Fetal Diagn Ther 2015.71. Hubinont C, Bernard P, Pirot N, Biard J,Donnez J. Twin-to-twin transfusion syndrome:treatment by amniodrainage and septostomy.Eur J Obstet Gynecol Reprod Biol 2000;92:141-4.72. Kacerovsky M, Tosner J. Prenatal diagnosisof an intertwin membrane hematoma. J ClinUltrasound 2010;38:397-9.73. Jauniaux E, Nicolaides KH. Early ultrasounddiagnosis and follow-up of molar pregnancies.Ultrasound Obstet Gynecol 1997;9:17-21.

74. Wee L, Jauniaux E. Prenatal diagnosis andmanagement of twin pregnancies complicatedby a co-existing molar pregnancy. Prenat Diagn2005;25:772-4.75. Roescher AM, Timmer A, Erwich JJ,Bos AF. Placental pathology, perinatal death,neonatal outcome, and neurological develop-ment: a systematic review. PLoS One 2014;9:e89419.76. Ptacek I, Sebire NJ, Man JA, Brownhill P,Hazell AEP. Systematic review of placental pa-thology reported in association with stillbirth.Placenta 2014;35:552-62.77. Katzman PJ. Chronic Inflammatory lesionsof the placenta. Semin Perinatol 2015;39:20-6.78. Kent EM, Breathnach FM, Gillan JE, et al.Placental pathology, birthweight discordance,and growth restriction in twin pregnancy: resultsof the ESPRiT Study. Am J Obstet Gynecol2012;207:220.e1-5.79. Eberle AM, Levesque D, Vintzileos AM,Egan JF, Tsapanos V, Salafia CM. Placentalpathology in discordant twins. Am J ObstetGynecol 1993;169:931-5.80. Chan MP, Hecht JL, Kane SE. Incidenceand clinicopathologic correlation of fetal vesselthrombosis in mono- and dichorionic twin pla-centas. J Perinatol 2010;30:660-4.81. Young BC, Wylie BJ. Effects of twin gesta-tion on maternal morbidity. Semin Perinatol2012;36:162-8.82. Weis MA, Harper LM, Roehl KA, Odibo AO,Cahill AG. Natural history of placenta previa intwins. Obstet Gynecol 2012;120:753-8.83. Romundstad LB, Romundstad PR,Sunde A, von During V, Skjaerven R,Vatten LJ. Increased risk of placenta previain pregnancies following IVF/ICSI; a com-parison of ART and non-ART pregnancies inthe same mother. Hum Reprod 2006;21:2353-8.84. Jauniaux E, Jurkovic D. Placenta accreta:pathogenesis of a 20th century iatrogenic uter-ine disease. Placenta 2012;33:244-51.85. Topuz S. Spontaneous uterine rupture at anunusual site due to placenta percreta in a 21-week twin pregnancy with previous cesareansection. Clin Exp Obstet Gynecol 2004;31:239-41.86. Patsouras K, Panagopoulos P, Sioulas V,Salamalekis G, Kassanos D. Uterine rupture at17 weeks of a twin pregnancy complicated withplacenta percreta. J Obstet Gynaecol 2010;30:60-1.87. NagyPS. Spontaneous rupture of the uteruscaused by placenta percreta at 28 weeks of twinpregnancy. Eur J Obstet Gynecol Reprod Biol2003;111:207-9.88. Ananth CV, Oyelese Y, Yeo L, Pradhan A,Vintzileos AM. Placental abruption in the UnitedStates, 1979 through 2001: temporal trends andpotential determinants. Am J Obstet Gynecol2005;192:191-8.89. Ananth CV, Smulian JC, Demissie K,Vintzileos AM, Knuppel RA. Placental abruptionamong singleton and twin births in the United

OCTOBER 2015 Am

States: risk factor profiles. Am J Epidemiol2001;153:771-8.90. Ananth CV, Smulian JC, Srinivas N,Getahun D, Salihu HM. Risk of infant mortalityamong twins in relation to placental abruption:contributions of preterm birth and restrictedfetal growth. Twin Res Hum Genet 2005;8:524-31.91. Aliyu MH, Alio AP, Lynch O, Mbah A,Salihu HM.Maternal pre-gravid bodyweight andrisk for placental abruption among twin preg-nancies. J Matern Fetal Neonatal Med 2009;22:745-50.92. McPherson JA, Odibo AO, Shanks AL,Roehl KA, Macones GA, Cahill AG. Adverseoutcomes in twin pregnancies complicated byearly vaginal bleeding. Am J Obstet Gynecol2013;208:56.e1-5.93. Fries MH, Goldstein RB, Kilpatrick SJ,Golbus MS, Callen PW, Filly RA. The role ofvelamentous cord insertion in the etiology oftwin-twin transfusion syndrome. ObstetGynecol1993;81:569-74.94. Lopriore E, Sueters M, Middeldorp JM,Oepkes D, Walther FJ, Vandenbussche FP.Velamentous cord insertion and unequal pla-cental territories in monochorionic twins withand without twin-to-twin-transfusion syn-drome. Am J Obstet Gynecol 2007;196:159.e1-5.95. Costa-Castro T, De Villiers S, Montenegro N,et al. Velamentous cord insertion in mono-chorionic twins with or without twin-twin trans-fusion syndrome: Does it matter? Placenta2013;34:1053-8.96. DePaepeME, Shapiro S, Hanley LC, Chu S,Luks FI. Correlation between cord insertion typeand superficial choriovasculature in diamniotic-monochorionic twin placentas. Placenta 2011;32:901-5.97. Gavriil P, Jauniaux E, Leroy F. Pathologicexamination of placentas from singleton andtwin pregnancies obtained after in vitro fertiliza-tion and embryo transfer. Pediatr Pathol1993;13:453-62.98. Baulies S, Maiz N, Muñoz A, et al. Prenatalultrasound diagnosis of vasa previa and analysisof risk factors. Prenat Diagn 2007;27:595-9.99. BronsteenR,WhittenA,BalasubramanianM,et al. Vasa previa: clinical presentations, out-comes, and implications for management. Obs-tet Gynecol 2013;122:352-7.100. Heifetz SA. Single umbilical artery: a sta-tistical analysis of 237 autopsy cases and reviewof the literature. Perspect Pediatr Pathol 1984;8:345-78.101. Klatt J, Kuhn A, BaumannM, Raio L. Singleumbilical artery in twin pregnancies. UltrasoundObstet Gynecol 2012;39:505-9.102. Stout MJ, Odibo AO, Longman R,Shanks AL, Cahill AG. The incidence of isolatedsingle umbilical artery in twins and adversepregnancy outcomes. Prenat Diagn 2013;33:269-72.103. Byers BD, Saade GR, Harirah HM. Twinpregnancies discordant for single umbilicalartery. J Reprod Med 2013;58:241-5.











































































































































































































http://www.AJOG.org


104. Beaudet L, Karuri S, Lau J, Magee F,Lee SK, von Dadelszen P. Placental pathologyand clinical outcomes in a cohort of infantsadmitted to a neonatal intensive care unit.J Obstet Gynecol Can 2007;29:315-23.105. Chang KT. Examination of the placenta:medico-legal implications. Semin Fetal NeonatalMed 2014;19:279-84.106. Fox H, Sebire NJ. Pathology of theplacenta, 3rd ed. Philadelphia: Elsevier; 2007.107. De Paepe ME, Shapiro S, Young L, Luks FI.Placental characteristics of selective birth weight

S102 American Journal of Obstetrics & Gynecolog

discordance in diamnioticemonochorionic twinsgestations. Placenta 2010;31:380-6.108. Salafia CM, Charles AK, Maas EM.Placenta and fetal growth restriction. Clin ObstetGynecol 2006;49:236-56.109. Risnes KR, Romundstad PR, Nilsen TI,Eskild A, Vatten LJ. Placental weight relativeto birth weight and long-term cardiovascularmortality: findings from a cohort of 31,307 menand women. Am J Epidemiol 2009;170:622-31.110. Almog B, Shehata F, Aljabri S, Levin I,Shalom-Paz E, Shrim A. Placenta weight

y OCTOBER 2015

percentile curves for singleton and twins de-liveries. Placenta 2011;32:58-62.111. Lao TT, Wong WM. Implications of ahigh placental ratio in pregnancies withappropriate-for-gestational age neonates.Gynecol Obstet Invest 2001;52:34-7.112. De Paepe ME, Shapiro S, Young LE,Luks FI. Placental weight, birth weight and fetal:placental weight ratio in dichorionic and mono-chorionic twin gestations in function of gesta-tional age, cord insertion type and placentalpartition. Placenta 2015;36:213-20.





































http://www.AJOG.org

Date post:	08-Jun-2018
Category:	Documents
Upload:	trancong
View:	223 times
Download:	0 times

Anomalies of the placenta and umbilical cord in twin...

Documents