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BSTETRICS
linical outcome in neonates with twinnemia-polycythemia sequence
nrico Lopriore, MD, PhD; Femke Slaghekke, MD; Dick Oepkes, MD, PhD; Johanna M. Middeldorp, MD, PhD;rank P. Vandenbussche, MD, PhD; Frans J. Walther, MD, PhD
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BJECTIVE: The purpose of this study was to evaluate neonatal out-ome of monochorionic twin pregnancies complicated by twin anemia-olycythemia sequence (TAPS).
TUDY DESIGN: A cohort of consecutive monochorionic twins withAPS with double survivors was included in the study. Each twin pairith TAPS was compared with 2 monochorionic twin pairs who werenaffected by TAPS or twin-to-twin transfusion syndrome and whoere matched for gestational age at birth. Neonatal death, severe mor-
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4.e1 American Journal of Obstetrics & Gynecology JULY 2010
ESULTS: We included19 twinpairs in theTAPSgroupand38control twinairs. The incidence of neonatal death and severe neonatal morbidity wasimilar in the TAPS group and control group (3% [1/38] vs 1% [1/76] and4% [9/38] vs 28% [21/76], respectively). Severe cerebral injury was de-
ected in 1 infant (5%) in the TAPS group and 1 infant (2%) in the control group.
ONCLUSION: Neonatal mortality and morbidity rates in a select popu-ation of TAPS neonates are similar to control neonatal rates.
ey words: anemia, monochorionic twins, polycythemia, twin
idity, and cerebral injury were studied. anemia-polycythemia sequence, twin-twin transfusion syndromeite this article as: Lopriore E, Slaghekke F, Oepkes D, et al. Clinical outcome in neonates with twin anemia-polycythemia sequence. Am J Obstet Gynecol
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etofetal blood transfusion occurs inall monochorionic twins because of
he invariable presence of placental vas-ular anastomoses and can lead to severeomplications. The best-known clinicalyndrome is twin-twin transfusion syn-rome (TTTS). TTTS is characterized byhe presence of oligohydramnios in the
rom the Division of Neonatology,epartment of Pediatrics (Drs Lopriore andalther), and the Division of Fetaledicine, Department of Obstetrics (Drs
laghekke, Oepkes, Middeldorp, andandenbussche), Leiden University Medicalentre, Leiden, the Netherlands.
resented at the 28th Annual Meeting of thenternational Fetal Medicine and Surgeryociety, Amazon, Brazil, Sept. 6-10, 2009, andt the 4th Annual Symposium ononochorionic Multiple Pregnancies of theurofetus group, Barcelona, Spain, May 22-3, 2009.
eceived Sept. 25, 2009; revised Oct. 29,009; accepted Feb. 10, 2010.
eprints not available from the authors.
uthorship and contribution to the article isimited to the 6 authors indicated. There waso outside funding or technical assistance withhe production of this article.
002-9378/$36.002010 Mosby, Inc. All rights reserved.
onor and polyhydramnios in the recip-ent twin, the so-called twin oligopolyhy-ramnios sequence (TOPS).1 Recently,e described a new atypical form of
hronic fetofetal blood transfusion,ermed twin anemia-polycythemia se-uence (TAPS).2,3 TAPS is characterizedy the presence of large intertwin hemo-lobin difference without the degree ofmniotic fluid discordance (TOPS) thats required for the diagnosis of TTTS.2,3
APS may occur after laser surgery forTTS (post–laser surgery form) in up to3% of cases.4 In these post–laser surgeryAPS cases, it is usually the former recip-
ent who becomes anemic, whereas theormer donor becomes polycythemic.4,5
APS may also occur in approximately-5% of “uncomplicated” monochori-nic twin pregnancies (spontaneousorm).6,7
Both spontaneous and post–laser sur-ery TAPS have a similar anatomic sub-trate that is based on the presence ofnly few minuscule arteriovenous pla-ental vascular anastomoses, in thebsence of superficial arterioarterialnastomoses.2,8,9 These few minusculerteriovenous anastomoses lead to alow, chronic intertwin blood transfu-ion2,9 that allows more time for hemo-
ory mechanisms n
nd may prevent dysregulation of hor-onal systems and the development ofOPS.10
TAPS can be diagnosed antenatallyith predefined Doppler-ultrasound
riteria4 or postnatally with hematologicriteria in combination with placentalnjection studies.6 Postnatal diagnosis ofAPS is based on the presence of chronicnemia (with highly increased reticulo-yte count) in the donor and polycythe-ia in the recipient in association with
ypical placental angioarchitecture afternjection with colored dye.6,8
Various studies have shown thatonochorionic twins with TTTS have
n increased risk for neonatal morbidity,erebral injury, and neurodevelopmentmpairment.11-13 Whether monochori-nic twins with TAPS are also at risk for
ncreased short-term neonatal morbid-ty or long-term neurodevelopment im-airment is not known. To date, out-ome in TAPS is based on few caseeports.2,9,14 We hypothesized that neo-atal morbidity TAPS cases with doubleurvivors is limited mainly to short-erm hematologic complications with-ut other severe complications. The aimf this study was to determine the neo-atal outcome in a large series of neo-
ates with TAPS in comparison with a
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www.AJOG.org Obstetrics Research
ontrol group of monochorionic twinsithout TAPS.
ATERIALS AND METHODS
ll consecutive monochorionic twinairs with TAPS who were admitted tour neonatal nursery at the Leiden Uni-ersity Medical Centre (The Nether-ands) between June 2002 and February009 were included in the study. Ourenter is an academic referral center thatanages all types of complications ofonochorionic pregnancies and the na-
ional center for invasive fetal therapy.bsence of antenatal signs of TOPS is anbsolute and fundamental condition forhe diagnosis of TAPS.6
For the purpose of this study, defini-ive diagnosis of TAPS was based onostnatal criteria. Postnatal criteria wereet if hematologic investigations at
irth showed chronic anemia in the do-or (hemoglobin, �5th percentile)15,16
nd polycythemia in the recipient (he-atocrit, �65%) in combination with
lacental injection studies that showednly small arteriovenous anastomosesdiameter, �1 mm) and no superficialrterioarterial anastomoses.8 We ex-luded all twin pregnancies with singler double intrauterine death and casesith an incomplete placental injection
tudy. TAPS cases (whether spontaneousr post–laser surgery TAPS cases) whoere treated subsequently with feto-
copic laser surgery were excluded fromhe study.
Details on the technique that has beensed for placental injection and placental
erritory measurement have been de-cribed previously.8 Part of the placentalata reported in this study were included
n a previous report on placental angio-rchitecture in TAPS.8 Two spontaneousAPS cases2 and 2 post–laser surgeryAPS cases were published previously.3,9
Each twin pair with TAPS was com-ared with 2 control monochorionicwin pairs who were unaffected by TAPSr TTTS and matched by gestational aget birth (� 1 week gestation).
We recorded the gestational age atirth, birthweight, and intertwin birth-
eight discordance.12 Gestational age at celivery was assigned by ultrasound dat-ng during the first trimester.
Hemoglobin levels and reticulocyteount were measured routinely at birthn all monochorionic twins. Blood sam-lings were obtained primarily frommbilical cord blood. If cord blood wasot available, samplings were obtainedoutinely on day 1 through heel stick orenous puncture. Anemia at birth wasefined as a hemoglobin level at �5thercentile for gestational age.15,16 Poly-ythemia-hyperviscosity syndrome wasefined as a hematocrit level of �65%.riteria for blood transfusion and partial
xchange transfusion remained un-hanged during the study period.
Cranial ultrasound scans were per-ormed in all neonates according to ournit protocol, which requires a mini-um of 3 scans during the first week of
ife (days 1, 3, and 7), followed by weeklycans thereafter until discharge or trans-er to another hospital. Intraventricularemorrhage with or without parenchy-al involvement was graded according
o the classification of Volpe,17 anderiventricular leukomalacia was gradedccording to the classification of de Vriest al.18 Ventricular dilation was diag-osed when measurement of the lateralentricles exceeded the 97th percentile,ith the use of ventricular index mea-
urements as described by Levene.19 Se-ere cerebral lesions on ultrasound scansere defined as the presence of at least 1f the following findings: intraventricu-
ar hemorrhage grade III, intraventricu-ar hemorrhage with parenchymalnvolvement, cystic periventricular leu-omalacia � grade II, ventricular dila-ion, porencephalic or parenchymalysts, or other severe cerebral lesions thatere associated with adverse neurologicutcome. We recorded the followingeonatal morbidity: respiratory distressyndrome, chronic lung disease defined asxygen dependency at 36 weeks post-enstrual age, symptomatic patent duc-
us arteriosus that required medical ther-py or surgical closure, necrotizingnterocolitis of stage II or more, and ret-nopathy of prematurity of stage III or
ore. Liver and/or renal function testsere performed in case of clinical suspi-
ion for liver or renal complications. (
JULY 2010 Ameri
imilarly, echocardiography was noterformed routinely, only based on clin-
cal suspicion for cardiac anomaly.Primary outcome was a composite
utcome measure, termed severe neona-al morbidity and defined as any of theollowing: respiratory distress syn-rome, chronic lung disease, patent duc-us arteriosus, necrotizing enterocolitisf stage II or more, retinopathy of pre-aturity of stage III or more, or severe
erebral lesions. Because of the retro-pective and observational nature of thistudy, our local ethical committee statedhat the study was exempt from institu-ional review board approval, accordingo Dutch legislation.
Clinical characteristics and neonatalutcome were compared between theAPS and control group. Results of cat-goric variables were compared with these of Fisher’s exact test. Normally dis-
ributed continuous variables were ana-yzed with the unpaired Student t test. Arobability value of � .05 was consid-red to indicate statistical significance.nalysis was performed with SPSS soft-are (version 16; SPSS Inc, Chicago, IL).
ESULTSuring the study period, 244 TTTS casesere treated with fetoscopic laser sur-ery at our center. Single or double fetaleath after laser surgery occurred in 5523%) and 32 (13%) TTTS pregnancies,espectively. In the remaining 157 TTTSregnancies with double survival atirth, 15 cases (10%) fulfilled the post-atal criteria of TAPS and were included
n this study. One post–laser surgeryAPS case was excluded because of theresence of a (small) superficial arterio-rterial anastomosis on placental injec-ion.9 During the same study period, 152ncomplicated monochorionic twinsere born at our center. Five twin pairs
3%) fulfilled the postnatal criteria forAPS. Two spontaneous TAPS cases thatere detected antenatally were treatedith fetoscopic laser surgery after diag-osis and were excluded from the study.n total, 19 consecutive twin pairs ful-lled the criteria for TAPS and were in-luded in the study. Fourteen cases
74%) were post–laser surgery TAPS,can Journal of Obstetrics & Gynecology 54.e2
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5
nd 5 cases (26%) were spontaneousAPS cases.Doppler measurements of the middle
erebral artery-peak systolic flow veloc-ty from both fetuses were available from9% of cases (15/19) in the TAPS group.ncreased middle cerebral artery-peakystolic flow velocity in the donor inombination with a decreased middleerebral artery-peak systolic flow veloc-ty in the recipient was detected antena-ally in 60% of these cases (9/15). The
ean gestational age at laser surgery inhe 14 cases of post–laser surgery TAPSases was 20.0 weeks (SD, 3.9 weeks).he mean gestational age at detection ofAPS in the 9 antenatally detected post–
aser surgery TAPS cases was 25.0 weeks.n 10 of the 14 postlaser surgery TAPSases (71%), the former recipient wasnemic at birth (ie, had become the newonor after laser surgery).Baseline characteristics in the groupith and without TAPS are presented inable 1.Neonatal mortality and morbidity
ates in both groups are presented in Ta-le 2. Neonatal death occurred in 2 cases,in each group. The neonate that died in
he TAPS group was an extensor of aregnancy with TTTS that had beenreated by laser surgery. Fetal magneticesonance imaging that was performed 1onth after laser surgery showed signif-
cant symmetric parenchymal loss that
TABLE 1Baseline characteristics in infants
Characteristic
Gestational age at birth, wka
...................................................................................................................
Female, n (%)...................................................................................................................
Vaginal delivery, n (%)...................................................................................................................
Birthweight, gb...................................................................................................................
Birthweight discordance, %b
...................................................................................................................
Small for gestational age, n (%)...................................................................................................................
Placenta with only small arteriovenousanastomoses, n (%)c...................................................................................................................
Placenta with arterioarterial anastomoses, n (...................................................................................................................a Data are given as mean � SD (range); b Data are given as m
Lopriore. Twin anemia-polycythemia sequence. Am J Obs
as especially prominent at the parietal
4.e3 American Journal of Obstetrics & Gynecolog
nd occipital lobes, together with aarked enlargement of both ventricles
nd pericerebral space. At birth at 36eeks of gestation, his weight was 1165 g,
nd his head circumference was 24 cm,oth �2 SD. Cerebral ultrasound exam-
nation and postnatal cerebral magneticesonance imaging confirmed the ante-atal findings of bilateral atrophic pa-enchymal lesions. In addition, extensiveolymicrogyria and corpus callosumgenesia were found. The cause of the se-
h twin anemia-polycythemia sequenGroup
Twin anemia-polycythemia sequence(pregnancies, 19; neonates, 38)
32 � 2.8 (26–36).........................................................................................................................
16 (42).........................................................................................................................
10 (53).........................................................................................................................
1591 � 415.........................................................................................................................
14 � 14.........................................................................................................................
2 (5).........................................................................................................................
19 (100)
.........................................................................................................................
0.........................................................................................................................
� SD; c Differences between both groups are statistically signifi
ynecol 2010.
TABLE 2Clinical characteristics in twin anesequence neonates and control neo
Characteristic
Group
Twin aseque
Respiratory distress syndrome 9 (24...................................................................................................................
Chronic lung disease 1 (3)...................................................................................................................
Patent ductus arteriosus 0...................................................................................................................
Necrotizing enterocolitis � stage II 0...................................................................................................................
Severe cerebral injury 1 (3)a...................................................................................................................
Blood transfusion on day 1 15 (40...................................................................................................................
Partial exchange transfusion 13 (34...................................................................................................................
Severe neonatal morbidity 9 (24...................................................................................................................
Neonatal death 1 (3)a...................................................................................................................
Severe neonatal morbidity was defined as any of the followindisease, patent ductus arteriosus, necrotizing enterocolitis of sor severe cerebral injury.a The infant in the twin anemia-polycythemia sequence group
Lopriore. Twin anemia-polycythemia sequence. Am J Obstet G
y JULY 2010
ere cerebral lesions was unclear butould be due to a hypoxic event before oruring laser treatment. The infant diedf respiratory failure on day 2. The neo-ate who died in the control group waseverely growth-restricted (birthweight80 g at 27 weeks of gestation) and diedf respiratory failure on day 2.Hematologic complications at birthere almost ubiquitous in the TAPSroup and rare in the control group.lood transfusion at birth was required
and control infants
Control (pregnancies, 38 pregnancies;neonates, 76)
32.2 � 2.7 (26–36)..................................................................................................................
40 (53)..................................................................................................................
18 (47)..................................................................................................................
1780 � 521..................................................................................................................
15 � 14..................................................................................................................
4 (5)..................................................................................................................
0
..................................................................................................................
36 (95%)..................................................................................................................
(P � .05).
a-polycythemiates
(%)
P valuemia-polycythemia(n � 38)
Control(n � 76)
18 (24) 1.0..................................................................................................................
2 (3) 1.0..................................................................................................................
4 (5) .30..................................................................................................................
6 (8) .18..................................................................................................................
1 (1) 1.0..................................................................................................................
2 (3) � .01..................................................................................................................
1 (1) � .01..................................................................................................................
21 (28) .82..................................................................................................................
1 (1) 1.0..................................................................................................................
aracteristics: respiratory distress syndrome, chronic lungII or more, retinopathy of prematurity of stage III or more,
died was the same as the infant with severe cerebral injury.
wit ce
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n 80% of donors (15/19). None of thesenfants were treated with erythropoietin.artial exchange transfusion for polycy-
hemia-hyperviscosity syndrome was re-uired in 68% of recipients (13/19). In5% of TAPS twin pairs (18/19), either alood transfusion or a partial exchangeransfusion was required on day 1. In 1APS twin pair who were born at 33eeks of gestation, the donor was ane-ic (hemoglobin, 10.5 g/dL), and the re-
ipient was polycythemic (hematocrit,9%); both infants were asymptomatict birth and did not require additionalreatment. In the control group, 2 neo-ates (3%) required a blood transfusionn day 1, and 1 polycythemic neonate1%) required a partial exchange trans-usion. In 5% of control twin pairs (2/8), either a blood transfusion or a par-ial exchange transfusion was requiredn day 1. In 1 control twin pair who wereorn at 35 weeks of gestation, the firstwin was anemic (hemoglobin, 12.5/dL) but did not require a blood trans-usion; the second-twin was polycythe-
ic (hemoglobin, 23.8 g/dL; hematocrit,3%) and needed a partial exchangeransfusion. The anemic twin had nor-
al reticulocyte count (5.7%), and
TABLE 3Results of cranial ultrasound exampolycythemia sequence neonates a
Variable
Group
Twinpolycsequ
Intraventricular hemorrhage..........................................................................................................
Grade I 2 (5..........................................................................................................
Grade II 2 (5..........................................................................................................
Grade III 0...................................................................................................................
Intraparenchymatous echodensity 0...................................................................................................................
Persistent periventricularechodensities
11 (2
...................................................................................................................
Cystic periventricular leukomalacia� grade II
0
...................................................................................................................
Ventricular dilation 0...................................................................................................................
Lenticulostriate vasculopathy 2 (5...................................................................................................................
Severe cerebral injury 1 (3...................................................................................................................
Lopriore. Twin anemia-polycythemia sequence. Am J Obs
lacental injection showed a large arte- t
ioarterial anastomosis. Both factorsrecluded the presence of TAPS andere suggestive of an acute form of fet-fetal transfusion. In addition, throm-ocytopenia (platelet count, �150 �09/L) occurred more often in the TAPSroup than in the control group (45%17/38] and 11% [11/38], respectively;
� .01). In the TAPS group, plateletount was significantly lower in recipi-nts than in donors (133 � 109/L and18 � 109/L, respectively; P � .01). Oneecipient twin had clinically significantevere thrombocytopenia (24 � 109/L)hat required a platelet transfusion atirth. Detailed information and analysisf hematologic findings in this popula-ion is described separately.20
Cranial ultrasound scans were per-ormed at least once in all infants in bothroups. The incidence of cerebral lesionshat were detected on ultrasound scansas similar in the TAPS group and con-
rol infants (Table 3).
OMMENThis study shows that neonatal deathnd severe neonatal morbidity in a selectroup of neonates with TAPS is similar
tions in twin anemia-control neonates(%)
P value
mia-emiae (n � 38)
Control group(n � 76)
..................................................................................................................
3 (4) 1.0..................................................................................................................
0 .11..................................................................................................................
1 (1) 1.0..................................................................................................................
0 —..................................................................................................................
15 (20) .34
..................................................................................................................
0 —
..................................................................................................................
1 (1) 1.0..................................................................................................................
4 (5) 1.0..................................................................................................................
1 (1) 1.0..................................................................................................................
ynecol 2010.
o a control group of monochorionic f
JULY 2010 Ameri
wins who were matched for gestationalge. Moreover, the incidence of minornd major cerebral lesions was similar inoth groups. Neonates with TAPS haveainly short-term hematologic compli-
ations that require blood transfusionst birth (for the anemic donor) or partialxchange transfusions (for the polycy-hemic recipient). Our data suggest that,lthough chronic fetofetal transfusion inAPS leads to short-term hematologicorbidities at birth, it does not seem to
ffect other organ systems.The absence of increased neonatalorbidity in TAPS is in contrast with the
igh rate of neonatal complications thatre reported in TTTS. In previous stud-es, we have shown that the incidence ofeonatal morbidities and cerebral injury
n TTTS was significantly increasedompared with a control group of un-omplicated monochorionic twins.12,21
ive-born infants with TTTS, particu-arly if not treated with fetoscopic laserurgery, are at high risk for extreme pre-
aturity and cardiac, renal, and cerebralnjury. Although the risk of hematologicomplications in TTTS is still presentven after laser surgery,12,21 hematologiciscordances at birth are less frequenthan after TAPS. The cause of the neona-al morbidities encountered in TTTS iselated to the severe fetal hemodynamiclterations typically seen in TTTS.10 Wepeculate that the low rate of neonatal
orbidities in TAPS may be related to ailder form of hemodynamic alteration
uring fetal life, in contrast with TTTS.When our results are interpreted, sev-
ral methods limitations of the studyhould be considered, such as its retro-pective nature and the small sampleize, which are inherent to the rarity ofhe disease. Moreover, for the purpose ofhis study, only cases with double liveirths and complete placental investiga-ion were included. These strict criteriaere used to ascertain the presence ofAPS and to select a homogeneous pop-lation. However, TAPS is also known to
ead to single or double fetal death.4,22
his may have led to a selection towardsilder cases of TAPS. The true impact of
inand, n
aneythenc
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etal and neonatal outcome in TAPS can
can Journal of Obstetrics & Gynecology 54.e4
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5
e determined only through prospectiveongitudinal studies that start as soon asAPS is detected during fetal life.Whether absence of increased short-
erm morbidity in TAPS also leads to fa-orable long-term outcome is not clear.imited data are available on the long-erm neurodevelopment impairment inAPS. In a large multicenter long-term
ollow-up study of 212 TTTS pregnan-ies that were treated with laser surgery,6 pregnancies (4%) were affected byAPS.22 Perinatal survival in these 16ostlaser surgery TAPS cases was 75%12/16). There were 2 fetal deaths and 2eonatal deaths. All 12 surviving TAPS
nfants were evaluated at 2 years of ageith a complete follow-up examination
hat included a Bayley developmentalest. None of these infants had long-termeurodevelopment impairment. Moreesearch is needed to determine the long-erm follow-up results at school age.
In conclusion, our findings suggesthat the incidence of neonatal death andevere neonatal morbidity in this selectopulation of TAPS is similar to control
nfants. Neonatal morbidity in TAPSeems to be limited to mainly short-erm hematologic complications. Im-ortantly, these results and conclusionshould be interpreted with care becausehey apply only to TAPS with double sur-ivors at birth. Complications rates inAPS could be higher because this studyas not able to exclude (late) pregnancyorbidity or death. Given the small size
f this study, larger prospectively col-ected data series (ideally through an in-ernational registry) are warranted toeach firmer conclusions. f
EFERENCES. Huber A, Hecher K. How can we diagnose
nd manage twin-twin transfusion syndrome? O4.e5 American Journal of Obstetrics & Gynecolog
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ate through a single placental arterio-venousnastomosis in a monochorionic twin preg-ancy. Placenta 2009;30:223-5.. Robyr R, Lewi L, Salomon LJ, et al. Preva-
ence and management of late fetal complica-ions following successful selective laser coag-lation of chorionic plate anastomoses in twin-o-twin transfusion syndrome. Am J Obstetynecol 2006;194:796-803.. van den Wijngaard JP, Lewi L, Lopriore E, etl. Modeling severely discordant hematocritsnd normal amniotic fluids after incomplete la-er therapy in twin-to-twin transfusion syn-rome. Placenta 2007;28:611-5.. Lopriore E, Oepkes D. Fetal and neonatalaematological complications in monochori-nic twins. Semin Fetal Neonatal Med008;13:231-8.. Lewi L, Jani J, Blickstein I, et al. The outcomef monochorionic diamniotic twin gestations inhe era of invasive fetal therapy: a prospectiveohort study. Am J Obstet Gynecol 2008;99:514-8.. Lopriore E, Deprest J, Slaghekke F, et al.lacental characteristics in monochorionic
wins with and without twin anemia-polycythe-ia sequence. Obstet Gynecol 2008;112:53-8.. Lopriore E, van den Wijngaard JP, Middel-orp JM, et al. Assessment of feto-fetal trans-
usion flow through placental arterio-venousnastomoses in a unique case of twin-to-twinransfusion syndrome. Placenta 2007;28:09-11.0. Lopriore E, Middeldorp JM, Sueters M,andenbussche FP, Walther FJ. Twin-to-twin
ransfusion syndrome: from placental anasto-oses to long-term neurodevelopmental out-
ome. Curr Pediatr Rev 2005;1:191-203.1. Lopriore E, Nagel HT, Vandenbussche FP,alther FJ. Long-term neurodevelopmental
utcome in twin-to-twin transfusion syndrome.m J Obstet Gynecol 2003;189:1314-9.2. Lopriore E, Sueters M, Middeldorp JM,
epkes D, Vandenbussche FP, Walther FJ.y JULY 2010
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